Skip to main content

Advertisement

Log in

Using functional traits to assess the influence of burrowing bivalves on nitrogen-removal in streams

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Functional traits define an organism in terms of how the organism interacts with its environment and determine the influence the organism has on dynamic ecosystem processes, such as biogeochemical nutrient cycling. Freshwater mussels (Bivalvia: Unionidae) form hotspots of biogeochemical activity in benthic environments by alleviating nutrient limitation at the sediment–water interface; however, little is known about the influence of mussel functional traits on sediment biogeochemical cycles, particularly nitrogen (N)-removal via denitrification and anammox. Our aim was to model the influence of two mussel functional traits: ammonium (NH4+) excretion and organic matter (OM) biodeposition, on N-removal in stream sediments. We quantified mussel excretion and biodeposition and incubated mussels in microcosms containing river sediment using flow-through methods. We measured nutrient and gas fluxes to quantify real-time ambient N-removal (denitrification + anammox), and conducted isotope pairing techniques to determine the maximum N-removal potential for denitrification and anammox pathways. NH4+ excretion was shown to be a significant predictor of ambient N-removal, whereas OM biodeposition significantly increased the maximum N-removal potential in the sediment. Our study is the first of its kind to link mussel functional traits specifically to N-removal and contributes to the growing knowledge of the role these highly imperiled organisms play by directly and indirectly influencing ecosystem-scale processes in lotic systems.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allen DC, Vaughn CC (2009) Burrowing behavior of freshwater mussels in experimentally manipulated communities. J N Am Benthol Soc 28:93–100

    Article  Google Scholar 

  • Allen DC, Vaughn CC, Kelly JF, Cooper JT, Engel MH (2012) Bottom-up biodiversity effects increase resource subsidy flux between ecosystems. Ecology 93:2165–2174

    Article  Google Scholar 

  • Amyot J-P, Downing JA (1991) Endo- and epibenthic distribution of the unionid mollusc Elliptio complanata. J N Am Benthol Soc 10:280–285

    Article  Google Scholar 

  • Anschutz P, Ciutat A, Lecroart P, Gérino M, Boudou A (2012) Effects of tubificid worm bioturbation on freshwater sediment biogeochemistry. Aquat Geochem 18:475–497

    Article  Google Scholar 

  • Atkinson CL, Vaughn CC (2015) Biogeochemical hotspots: temporal and spatial scaling of the impact of freshwater mussels on ecosystem function. Freshw Biol 60:563–574

    Article  Google Scholar 

  • Atkinson CL, Vaughn CC, Forshay KJ, Cooper JT (2013) Aggregated filter-feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics. Ecology 94:1359–1369

    Article  Google Scholar 

  • Atkinson CL, Kelly JF, Vaughn CC (2014) Tracing consumer-derived nitrogen in riverine food webs. Ecosystems 17:485–496

    Article  Google Scholar 

  • Atkinson CL, Capps KA, Rugenski AT, Vanni MJ (2017) Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev 92:2003–2023

    Article  Google Scholar 

  • Atkinson CL, Allen DC, Davis L, Nickerson ZL (2018) Incorporating ecogeomorphic feedbacks to better understand resiliency in streams: a review and directions forward. Geomorphology 305:123–140

    Article  Google Scholar 

  • Atkinson CL, van Ee BC, Lu Y, Zhong W (2019) Wetland floodplain flux: temporal and spatial availability of organic matter and dissolved nutrients in an unmodified river. Biogeochemistry 142:395–411

    Article  Google Scholar 

  • Benelli S, Bartoli M, Racchetti E, Moraes PC, Zilius M, Lubiene I, Fano EA (2017) Rare but large bivalves alter benthic respiration and nutrient recycling in riverine sediments. Aquat Ecol 51:1–16

    Article  Google Scholar 

  • Berner RA (1981) A new geochemical classification of sedimentary environments. J Sediment Res 51:359–365

    Google Scholar 

  • Bilkovic DM, Mitchell MM, Isdell RE, Schliep M, Smyth AR (2017) Mutualism between ribbed mussels and cordgrass enhances salt marsh nitrogen removal. Ecosphere 8:1–18

    Article  Google Scholar 

  • Blann KL, Anderson JL, Sands GR, Vondracek B (2009) Effects of agricultural drainage on aquatic ecosystems: a review. Crit Rev Environ Sci Technol 39:909–1001

    Article  Google Scholar 

  • Bogan AE (2007) Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. In: Balian EV et al (eds) Freshwater animal diversity assessment. Springer, Dordrecht, pp 139–147

    Chapter  Google Scholar 

  • Bonaglia S, Nascimento FA, Bartoli M, Klawonn I, Brüchert V (2014) Meiofauna increases bacterial denitrification in marine sediments. Nat Commun 5:5133–5142

    Article  Google Scholar 

  • Boulton AJ, Findlay S, Marmonier P, Stanley EH, Valett HM (1998) The functional significance of the hyporheic zone in streams and rivers. Annu Rev Ecol Syst 29:59–81

    Article  Google Scholar 

  • Bunn SE, Arthington AH (2002) Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity. Environ Manage 30:492–507

    Article  Google Scholar 

  • Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426

    Article  Google Scholar 

  • Cardinale BJ, Matulich KL, Hooper DU, Byrnes JE, Duffy E, Gamfeldt L, Balvanera B, O’Connor MI, Gonzalez A (2011) The functional role of producer diversity in ecosystems. Am J Bot 98:572–592

    Article  Google Scholar 

  • Carlsson MS, Glud RN, Petersen JK (2010) Degradation of mussel (Mytilus edulis) fecal pellets released from hanging long-lines upon sinking and after settling at the sediment. Can J Fish Aquat Sci 67:1376–1387

    Article  Google Scholar 

  • Carpenter SR, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8:559–568

    Article  Google Scholar 

  • Catallo WJ (1999) Hourly and daily variation of sediment redox potential in tidal wetland sediments. US Geological Survey, Biological Resources Division, Reston

    Google Scholar 

  • Chen Y (1998) The respiratory physiology and energy metabolism of freshwater mussels and their responses to lack of oxygen. Dissertation, Virginia Polytechnic Institute and State University

  • Covich AP, Palmer MA, Crowl TA (1999) The role of benthic invertebrate species in freshwater ecosystems: zoobenthic species influence energy flows and nutrient cycling. Bioscience 49:119–127

    Article  Google Scholar 

  • Covich AP, Austen MC, Bärlocher F, Chauvet E, Cardinale BJ, Biles CL, Inchausti P, Dangles O, Solan M, Gessner MO, Statzner B, Moss B (2004) The role of biodiversity in the functioning of freshwater and marine benthic ecosystems. Bioscience 54:767–775

    Article  Google Scholar 

  • Dalton CM, Flecker AS (2014) Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems. Oecologia 176:691–701

    Article  Google Scholar 

  • de Bello FF, Lavorel S, Díaz S, Harrington R, Cornelissen JHC, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, da Silva PM, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893

    Article  Google Scholar 

  • Díaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655

    Article  Google Scholar 

  • Ensign SH, Doyle MW (2005) In-channel transient storage and associated nutrient retention: evidence from experimental manipulations. Limnol Oceanogr 50:1740–1751

    Article  Google Scholar 

  • Ensign SH, Doyle MW (2006) Nutrient spiraling in streams and river networks. Biogeosci, J Geophys Res. https://doi.org/10.1029/2005JG000114

    Book  Google Scholar 

  • Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JBC, Marquis RJ, Oksanen L, Oksanen T, Paine RT, Pikitch EK, Ripple WJ, Sandin SA, Scheffer M, Schoener TW, Shurin JB, Sinclair ARE, Soulé ME, Virtanen R, Wardle DA (2011) Trophic downgrading of planet Earth. Science 333:301–306

    Article  Google Scholar 

  • Eyre BD, Rysgaard S, Dalsgaard T, Christensen PB (2002) Comparison of isotope pairing and N2: Ar methods for measuring sediment denitrification—assumption, modifications, and implications. Estuaries 25:1077–1087

    Article  Google Scholar 

  • Flynn DF, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity–ecosystem function relationships. Ecology 92:1573–1581

    Article  Google Scholar 

  • Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917–928

    Article  Google Scholar 

  • Giles H, Pilditch CA (2006) Effects of mussel (Perna canaliculus) biodeposit decomposition on benthic respiration and nutrient fluxes. Mar Biol 150:261–271

    Article  Google Scholar 

  • Grenz C, Hermin M-N, Baudinet D, Daumas R (1990) In situ biochemical and bacterial variation of sediments enriched with mussel biodeposits. Hydrobiologia 207:153–160

    Article  Google Scholar 

  • Grimm NB (1988) Role of macroinvertebrates in nitrogen dynamics of a desert stream. Ecology 69:1884–1893

    Article  Google Scholar 

  • Grimm NB, Sheibley RW, Crenshaw CL, Dahm CN, Roach WJ, Zeglin LH (2005) N retention and transformation in urban streams. J N Am Benthol Soc 24:626–642

    Article  Google Scholar 

  • Haag WR, Warren ML (2010) Diversity, abundance, and size structure of bivalve assemblages in the Sipsey River, Alabama. Aquat Conserv: Mar Freshw Ecosyst 20:655–667

    Article  Google Scholar 

  • Halvorson HM, Hall DJ, Evans-White MA (2017) Long-term stoichiometry and fates highlight animal egestion as nutrient repackaging, not recycling, in aquatic ecosystems. Funct Ecol 31:1802–1812

    Article  Google Scholar 

  • Higgins CB, Tobias C, Piehler MF, Smyth AR, Dame RF, Stephenson K, Brown BL (2013) Effect of aquacultured oyster biodeposition on sediment N2 production in Chesapeake Bay. Mar Ecol Prog Ser 473:7–27

    Article  Google Scholar 

  • Hoellein TJ, Zarnoch CB, Grizzle RE (2015) Eastern oyster (Crassostrea virginica) filtration, biodeposition, and sediment nitrogen cycling at two oyster reefs with contrasting water quality in Great Bay Estuary (New Hampshire, USA). Biogeochemistry 122:113–129

    Article  Google Scholar 

  • Hoellein TJ, Zarnoch CB, Bruesewitz DA, DeMartini J (2017) Contributions of freshwater mussels (Unionidae) to nutrient cycling in an urban river: filtration, recycling, storage, and removal. Biogeochemistry 135:307–324

    Article  Google Scholar 

  • Hölker F, Vanni MJ, Kuiper JJ, Meile C, Grossart HP, Stief P, Adrian R, Lorke A, Dellwig O, Brand A, Hupfer M, Mooij WM, Nützmann G, Lewandowski J (2015) Tube-dwelling invertebrates: tiny ecosystem engineers have large effects in lake ecosystems. Ecol Monogr 85:333–351

    Article  Google Scholar 

  • Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, Gonzalez A, Duffy JE, Gamfeldt L, O’Connor MI (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–109

    Article  Google Scholar 

  • Hou L, Liu M, Carini SA, Gardner WS (2012) Transformation and fate of nitrate near the sediment–water interface of Copano Bay. Cont Shelf Res 35:86–94

    Article  Google Scholar 

  • Jones HF, Pilditch CA, Bruesewitz DA, Lohrer AM (2011) Sedimentary environment influences the effect of an infaunal suspension feeding bivalve on estuarine ecosystem function. PLoS ONE 6:e27065

    Article  Google Scholar 

  • Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66:4166–4170

    Article  Google Scholar 

  • Kellogg ML, Cornwell JC, Owens MS, Paynter KT (2013) Denitrification and nutrient assimilation on a restored oyster reef. Mar Ecol Prog Ser 480:1–19

    Article  Google Scholar 

  • Knowles R (1982) Denitrification. Microbiol Rev 46:43–70

    Google Scholar 

  • Lautz L, Fanelli R (2008) Seasonal biogeochemical hotspots in the streambed around restoration structures. Biogeochemistry 91:85–104

    Article  Google Scholar 

  • Lavorel S, Garnier É (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556

    Article  Google Scholar 

  • Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli C, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  Google Scholar 

  • Matisoff G, Wang X (1998) Solute transport in sediments by freshwater infaunal bioirrigators. Limnol Oceanogr 43:1487–1499

    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 6:301–312

    Article  Google Scholar 

  • McGregor SW, O’Neil PE (1992) The biology and water-quality monitoring of the Sipsey River and Lubbub and Bear Creeks, Alabama, 1990-91. Geological Survey of Alabama, Biological Resources Division, vol. 169

  • Mermillod-Blondin F (2011) The functional significance of bioturbation and biodeposition on biogeochemical processes at the water–sediment interface in freshwater and marine ecosystems. J N Am Benthol Soc 30:770–778

    Article  Google Scholar 

  • Mermillod-Blondin F, Rosenberg R (2006) Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquat Sci 68:434–442

    Article  Google Scholar 

  • Miller-Way T, Twilley RR (1996) Theory and operation of continuous flow systems for the study of benthic-pelagic coupling. Mar Ecol Prog Ser 140:257–269

    Article  Google Scholar 

  • Mirto S, Danovaro R, Mazzola A (2000) Microbial and meiofaunal response to intensive mussel-farm biodeposition in coastal sediments of the western Mediterranean. Mar Pollut Bull 40:244–252

    Article  Google Scholar 

  • Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci 98:166–170

    Article  Google Scholar 

  • Newbold JD, Elwood JW, O’Neill RV, Winkle WV (1981) Measuring nutrient spiralling in streams. Can J Fish Aquat Sci 38:860–863

    Article  Google Scholar 

  • Newell RI, Cornwell JC, Owens MS (2002) Influence of simulated bivalve biodeposition and microphytobenthos on sediment nitrogen dynamics: a laboratory study. Limnol Oceanogr 47:1367–1379

    Article  Google Scholar 

  • Newell RI, Fisher T, Holyoke R, Cornwell J (2005) Influence of eastern oysters on nitrogen and phosphorus regeneration in Chesapeake Bay, USA. In: Dame RF, Olenin S (eds) The comparative roles of suspension-feeders in ecosystems. Springer, Dordrecht, pp 93–120

    Chapter  Google Scholar 

  • Nichols SJ, Silverman H, Dietz TH, Lynn JW, Garling DL (2005) Pathways of food uptake in native (Unionidae) and introduced (Corbiculidae and Dreissenidae) freshwater bivalves. J Great Lakes Res 31:87–96

    Article  Google Scholar 

  • Nizzoli D, Welsh DT, Bartoli M, Viaroli P (2005) Impacts of mussel (Mytilus galloprovincialis) farming on oxygen consumption and nutrient recycling in a eutrophic coastal lagoon. Hydrobiologia 550:183–198

    Article  Google Scholar 

  • Paetzold A, Schubert CJ, Tockner K (2005) Aquatic terrestrial linkages along a braided-river: riparian arthropods feeding on aquatic insects. Ecosystems 8:748–759

    Article  Google Scholar 

  • Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758

    Article  Google Scholar 

  • Poff N, Brinson MM, Day J (2002) Aquatic ecosystems and global climate change. Pew Center GlobClim Change, Arlington 44:1–36

    Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Ricciardi A, Rasmussen JB (1999) Extinction rates of North American freshwater fauna. Conserv Biol 13:1220–1222

    Article  Google Scholar 

  • Richter BD, Braun DP, Mendelson MA, Master LL (1997) Threats to imperiled freshwater fauna. Conserv Biol 11:1081–1093

    Article  Google Scholar 

  • Rusek J (1998) Biodiversity of Collembola and their functional role in the ecosystem. Biodivers Conserv 7:1207–1219

    Article  Google Scholar 

  • Schmitz OJ, Buchkowski RW, Burghardt KT, Donihue CM (2015) Functional traits and trait-mediated interactions: connecting community-level interactions with ecosystem functioning. Adv Ecol Res 52:319–343

    Article  Google Scholar 

  • Schwalb AN, Pusch MT (2007) Horizontal and vertical movements of unionid mussels in a lowland river. J N Am Benthol Soc 26:261–272

    Article  Google Scholar 

  • Seitzinger S, Harrison JA, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Drecht GV (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090

    Article  Google Scholar 

  • Smith E, Davison W, Hamilton-Taylor J (2002) Methods for preparing synthetic freshwaters. Water Res 36:1286–1296

    Article  Google Scholar 

  • Spooner DE, Vaughn CC (2006) Context-dependent effects of freshwater mussels on stream benthic communities. Freshw Biol 51:1016–1024

    Article  Google Scholar 

  • Spooner DE, Vaughn CC, Galbraith HS (2012) Species traits and environmental conditions govern the relationship between biodiversity effects across trophic levels. Oecologia 168:533–548

    Article  Google Scholar 

  • Strayer DL, Dudgeon D (2010) Freshwater biodiversity conservation: recent progress and future challenges. J N Am Benthol Soc 29:344–358

    Article  Google Scholar 

  • Strayer DL, Malcom HM (2007) Shell decay rates of native and alien freshwater bivalves and implications for habitat engineering. Freshw Biol 52:1611–1617

    Article  Google Scholar 

  • Strayer DL, Downing JA, Haag WR, King TL, Layzer JB, Newton TJ, Nichols SJ (2004) Changing perspectives on pearly mussels, North America’s most imperiled animals. Bioscience 54:429–439

    Article  Google Scholar 

  • Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318

    Article  Google Scholar 

  • Thrush SF, Hewitt JE, Gibbs M, Lundquist C, Norkko A (2006) Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9:1029–1040

    Article  Google Scholar 

  • Tilman D (2001) Functional diversity. Encyclopedia of Biodiversity 3:109–120

    Article  Google Scholar 

  • Tilman D, Knops J, Wedin D, Reich P, Ritchie M, Siemann E (1997) The influence of functional diversity and composition on ecosystem processes. Science 277:1300–1302

    Article  Google Scholar 

  • Trentman MT, Atkinson CL, Brant JD (2018) Native freshwater mussel effects on nitrogen cycling: impacts of nutrient limitation and biomass dependency. Freshwater Science 37:276–286

    Article  Google Scholar 

  • Turek KA, Hoellein TJ (2015) The invasive Asian clam (Corbicula fluminea) increases sediment denitrification and ammonium flux in 2 streams in the midwestern USA. Freshw Sci 34:472–484

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

    Article  Google Scholar 

  • Vaughn CC (2010) Biodiversity losses and ecosystem function in freshwaters: emerging conclusions and research directions. Bioscience 60:25–35

    Article  Google Scholar 

  • Vaughn CC (2017) Ecosystem services provided by freshwater mussels. Hydrobiologia 810:11–27

    Google Scholar 

  • Vaughn CC, Hakenkamp CC (2001) The functional role of burrowing bivalves in freshwater ecosystems. Freshw Biol 46:1431–1446

    Article  Google Scholar 

  • Vaughn CC, Spooner DE, Galbraith HS (2007) Context-dependent species identity effects within a functional group of filter-feeding bivalves. Ecology 88:1654–1662

    Article  Google Scholar 

  • Vaughn CC, Nichols SJ, Spooner DE (2008) Community and foodweb ecology of freshwater mussels. J N Am Benthol Soc 27:409–423

    Article  Google Scholar 

  • Vaughn CC, Atkinson CL, Julian JP (2015) Drought-induced changes in flow regimes lead to long-term losses in mussel-provided ecosystem services. Ecol Evol 5:1291–1305

    Article  Google Scholar 

  • Veuger B, Eyre BD, Maher D, Middelburg JJ (2007) Nitrogen incorporation and retention by bacteria, algae, and fauna in a subtropical, intertidal sediment: an in situ 15 N-labeling study. Limnol Oceanogr 52:1930–1942

    Article  Google Scholar 

  • Vidon P, Allan C, Burns D, Duval TP, Gurwick N, Inamdar S, Lowrance R, Okay J, Scott D, Sebestyen S (2010) Hot spots and hot moments in riparian zones: potential for improved water quality management. J Am Water Resour Assoc 46:278–298

    Article  Google Scholar 

  • Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116:882–892

    Article  Google Scholar 

  • Walker BH (1992) Biodiversity and ecological redundancy. Conserv Biol 6:18–23

    Article  Google Scholar 

  • Wallace JB, Webster JR (1996) The role of macroinvertebrates in stream ecosystem function. Annu Rev Entomol 41:115–139

    Article  Google Scholar 

  • Williams JD, Bogan AE, Garner JT (2008) Freshwater mussels of Alabama and the Mobile basin in Georgia, Mississippi, and Tennessee. University of Alabama Press, Tusaloosa

    Google Scholar 

  • Wilson MA, Carpenter SR (1999) Economic valuation of freshwater ecosystem services in the United States: 1971–1997. Ecol Appl 9:772–783

    Google Scholar 

Download references

Acknowledgements

Funding was provided by the University of Alabama, Dauphin Island Sea Lab, the Center for Freshwater Studies at University of Alabama, and through research grants awarded by the Birmingham Audubon Society and the Conchologists of America, Inc. Land access to the Sipsey River was granted by the Weyerhaeuser Company. For assistance in the field and lab, we thank Anne Bell, Alice Kleinhuizen, Corianne Tatariw, Brian van Ee, Anastasia Nickerson, Derek Tollette and Taylor Ledford.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zachary L. Nickerson.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Breck Bowden.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 96 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nickerson, Z.L., Mortazavi, B. & Atkinson, C.L. Using functional traits to assess the influence of burrowing bivalves on nitrogen-removal in streams. Biogeochemistry 146, 125–143 (2019). https://doi.org/10.1007/s10533-019-00612-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-019-00612-2

Keywords

Navigation