Ecosystems

pp 1–15 | Cite as

Consumer Aggregations Drive Nutrient Dynamics and Ecosystem Metabolism in Nutrient-Limited Systems

  • Carla L. Atkinson
  • Brandon J. Sansom
  • Caryn C. Vaughn
  • Kenneth J. Forshay
Article

Abstract

Differences in animal distributions and metabolic demands can influence energy and nutrient flow in an ecosystem. Through taxa-specific nutrient consumption, storage, and remineralization, animals may influence energy and nutrient pathways in an ecosystem. Here we show these taxa-specific traits can drive biogeochemical cycles of nutrients and alter ecosystem primary production and metabolism, using riverine systems that support heterogeneous freshwater mussel aggregations. Freshwater unionid mussels occur as distinct, spatially heterogeneous, dense aggregations in rivers. They may influence rates of production and respiration because their activities are spatially concentrated within given stream reaches. Previous work indicates that mussels influence nutrient limitation patterns, algal species composition, and producer and primary consumer biomass. Here, we integrate measures of organismal rates, stoichiometry, community-scaled rates, and ecosystem rates, to determine the relative source–sink nutrient dynamics of mussel aggregations and their influence on net ecosystem processes. We studied areas with and without mussel aggregations in three nitrogen-limited rivers in southeastern Oklahoma, USA. We measured respiration and excretion rates of mussels and collected a subset of samples for tissue chemistry and for thin sectioning of the shell to determine growth rates at each site. This allowed us to assess nutrient remineralization and nutrient sequestration by mussels. These rates were scaled to the community. We also measured stream metabolism at three sites with and without mussels. We demonstrated that mussel species have distinct stoichiometric traits, vary in their respiration rates, and that mussel aggregations influence nutrient cycling and productivity. Across all mussel aggregations, we found that mussels excreted more nitrogen than they sequestered into tissue and excreted more phosphorus than they sequestered except at one site. Furthermore, gross primary productivity was significantly greater at reaches with mussels. Collectively, our results indicate that mussels have ecosystem-level impacts on nutrient availability and production in nutrient-limited rivers. Within these streams, mussels are affecting the movement of nutrients and altering nutrient spiralling.

Keywords

stream metabolism remineralization unionid mussel stoichiometry nitrogen phosphorus nutrient storage gross primary productivity 

Supplementary material

10021_2017_166_MOESM1_ESM.docx (14 kb)
Supplementary material 1 (DOCX 14 kb)

References

  1. Allen DC, Vaughn CC, Kelly JF, Cooper JT, Engel M. 2012. Bottom-up biodiversity effects increase resource subsidy flux between ecosystems. Ecology 93:2165–74.CrossRefPubMedGoogle Scholar
  2. Allgeier JE, Yeager LA, Layman CA. 2013. Consumers regulate nutrient limitation regimes and primary production in seagrass ecosystems. Ecology 94:521–9.CrossRefPubMedGoogle Scholar
  3. Atkinson CL, Capps KA, Rugenski AT, Vanni MJ. 2017. Consumer-driven nutrient dynamics in freshwater ecosystems: from individuals to ecosystems. Biol Rev. doi:10.1111/brv.12318.
  4. Atkinson CL, Julian JP, Vaughn CC. 2014a. Species and function lost: role of drought in structuring stream communities. Biol Conserv 176:30–8.CrossRefGoogle Scholar
  5. Atkinson CL, Kelly JF, Vaughn CC. 2014b. Tracing consumer-derived nitrogen in riverine food webs. Ecosystems 17:485–96.CrossRefGoogle Scholar
  6. Atkinson CL, Vaughn CC. 2015. Biogeochemical hotspots: temporal and spatial scaling of the impact of freshwater mussels on ecosystem function. Freshw Biol 60:563–74.CrossRefGoogle Scholar
  7. Atkinson CL, Vaughn CC, Forshay KJ, Cooper JT. 2013. Aggregated filter-feeding consumers alter nutrient limitation: consequences for ecosystem and community dynamics. Ecology 94:1359–69.CrossRefPubMedGoogle Scholar
  8. Bogan AE. 1996. Decline and decimation: the extirpation of the unionid freshwater bivalves of North America. J Shellfish Res 15:484.Google Scholar
  9. Bogan AE. 2008. Global diversity of freshwater mussels (Mollusca, Bivalvia) in freshwater. Hydrobiologia 595:139–47.CrossRefGoogle Scholar
  10. Capps KA, Atkinson CL, Rugenski AT. 2015. Implications of species addition and decline for nutrient dynamics in fresh waters. Freshw Sci 34:485–96.CrossRefGoogle Scholar
  11. Capps KA, Flecker AS. 2013a. Invasive aquarium fish transform ecosystem nutrient dynamics. Proc R Soc B Biol Sci 280:20131520.CrossRefGoogle Scholar
  12. Capps KA, Flecker AS. 2013b. Invasive fishes generate biogeochemical hotspots in a nutrient-limited system. Plos One 8:e5403.CrossRefGoogle Scholar
  13. Castro AJ, Vaughn CC, García-Llorente M, Julian JP, Atkinson CL. 2016. Willingness to pay for ecosystem services among stakeholder groups in a South-Central US watershed with regional conflict. J Water Resour Plan Manag. 142:05016006.CrossRefGoogle Scholar
  14. Christian AD, Crump B, Berg DJ. 2008. Nutrient release and ecological stoichiometry of freshwater mussels (Mollusca:Unionidae) in 2 small, regionally distinct streams. J N Am Benthol Soc 27:440–50.CrossRefGoogle Scholar
  15. Clark G. 1980. Study of molluscan shell structure and growth lines using thin sections. In: Rhoads DC, Lutz RA, Eds. Skeletal growth of aquatic organisms. New York: Plenum Press. p 603–6.Google Scholar
  16. Culp JJ, Haag WR, Arrington DA, Kennedy TB. 2011. Seasonal and species-specific patterns in abundance of freshwater mussel glochidia in stream drift. J N Am Benthol Soc 30:436–45.CrossRefGoogle Scholar
  17. Dodds WK, Beaulieu JJ, Eichmiller JJ, Fischer JR, Franssen NR, Gudder DA, Makinster AS, McCarthy MJ, Murdock JN, O’Brien JM, Tank JL, Sheibley RW. 2008. Nitrogen cycling and metabolism in the thalweg of a prairie river. J Geophys Res Biogeosci 113:G04029.CrossRefGoogle Scholar
  18. Dodds WK, Veach AM, Ruffing CM, Larson DM, Fischer JL, Costigan KH. 2013. Abiotic controls and temporal variability of river metabolism: multiyear analyses of Mississippi and Chattahoochee River data. Freshw Sci 32:1073–87.CrossRefGoogle Scholar
  19. Doughty CE, Roman J, Faurby S, Wolf A, Haque A, Bakker ES, Malhi Y, Dunning JB, Svenning J-C. 2015. Global nutrient transport in a world of giants. Proc Natl Acad Sci 113:868–73.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW. 2000. Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–80.CrossRefPubMedGoogle Scholar
  21. Elser JJ, Urabe J. 1999. The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–51.CrossRefGoogle Scholar
  22. Flecker AS. 1996. Ecosystem engineering by a dominant detritivore in a diverse tropical stream. Ecology 77:1845–54.CrossRefGoogle Scholar
  23. Flecker AS, Taylor BW. 2004. Tropical fishes as biological bulldozers: density effects on resource heterogeneity and species diversity. Ecology 85:2267–78.CrossRefGoogle Scholar
  24. Galbraith HS, Frazier SE, Allison B, Vaughn CC. 2009. Comparison of gill surface morphology across a guild of suspension-feeding unionid bivalves. J Molluscan Stud 75:103–7.CrossRefGoogle Scholar
  25. Galbraith HS, Spooner DE, Vaughn CC. 2010. Synergistic effects of regional climate patterns and local water management on freshwater mussel communities. Biological Conservation 143:1175–83.CrossRefGoogle Scholar
  26. Golladay SW, Gagnon P, Kearns M, Battle JM, Hicks DW. 2004. Response of freshwater mussel assemblages (Bivalvia: Unionidae) to a record drought in the Gulf Coastal Plain of southwestern Georgia. J N Am Benthol Soc 23:494–506.CrossRefGoogle Scholar
  27. Haag WR. 2012. North American freshwater mussels: ecology, natural history, and conservation. New York (NY): Cambridge University Press.CrossRefGoogle Scholar
  28. Haag WR, Commens-Carson AM. 2008. Testing the assumption of annual shell ring deposition in freshwater mussels. Can J Fish Aquat Sci 65:493–508.CrossRefGoogle Scholar
  29. Haag WR, Rypel AL. 2011. Growth and longevity in freshwater mussels: evolutionary and conservation implications. Biol Rev 86:225–47.CrossRefPubMedGoogle Scholar
  30. Haag WR, Warren ML. 2003. Host fishes and infection strategies of freshwater mussels in large Mobile Basin streams, USA. J N Am Benthol Soc 22:78–91.CrossRefGoogle Scholar
  31. Haag WR, Warren ML. 2008. Effects of severe drought on freshwater mussel assemblages. Trans Am Fish Soc 137:1165–78.CrossRefGoogle Scholar
  32. Hall RO, Tank JL, Dybdahl MF. 2003. Exotic snails dominate nitrogen and carbon cycling in a highly productive stream. Front Ecol Environ 1:407–11.CrossRefGoogle Scholar
  33. Hill WR, Griffiths NA. 2016. Nitrogen processing by grazers in a headwater stream: riparian connections. Freshw Biol 62:17–29.CrossRefGoogle Scholar
  34. Hoellein TJ, Tank JL, Rosi-Marshall EJ, Entrekin SA, Lamberti GA. 2007. Controls on spatial and temporal variation of nutrient uptake in three Michigan headwater streams. Limnol Oceanogr 52:1964–77.CrossRefGoogle Scholar
  35. Holtgrieve GW, Schindler DE. 2011. Marine-derived nutrients, bioturbation, and ecosystem metabolism: reconsidering the role of salmon in streams. Ecology 92:373–85.CrossRefPubMedGoogle Scholar
  36. Holtgrieve GW, Schindler DE, Branch TA, A’mar ZT. 2010. Simultaneous quantification of aquatic ecosystem metabolism and reaeration using a Bayesian statistical model of oxygen dynamics. Limnol Oceanogr 55:1047–63.CrossRefGoogle Scholar
  37. Howard JK, Cuffey KM. 2006. The functional role of native freshwater mussels in the fluvial benthic environment. Freshw Biol 51:460–74.CrossRefGoogle Scholar
  38. Knapp AK, Blair JM, Briggs JM, Collins SL, Hartnett DC, Johnson LC, Towne EG. 1999. The keystone role of bison in North American tallgrass prairie—Bison increase habitat heterogeneity and alter a broad array of plant, community, and ecosystem processes. BioScience 49:39–50.CrossRefGoogle Scholar
  39. Kraft C. 1992. Estimates of phosphorus and nitrogen cycling by fish using a bioenergetics approach. Can J Fish Aquat Sci 49:2596–604.CrossRefGoogle Scholar
  40. Marzolf ER, Mulholland PJ, Steinman AD. 1994. Improvements to the diurnal upstream-downstream dissolved-oxygen change technique for determining whole-stream metabolism in small streams. Can J Fish Aquat Sci 51:1591–9.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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 89:2335–46.CrossRefPubMedGoogle Scholar
  43. McIntyre PB, Jones LE, Flecker AS, Vanni MJ. 2007. Fish extinctions alter nutrient recycling in tropical freshwaters. Proc Natl Acad Sci USA 104:4461–6.CrossRefPubMedPubMedCentralGoogle Scholar
  44. Moore JW. 2006. Animal ecosystem engineers in streams. BioScience 56:237–46.CrossRefGoogle Scholar
  45. Neves RJ, Moyer SN. 1988. Evaluation of techniques for age determination of freshwater mussels (Unionidae). Am Malacol Bull 6:179–88.Google Scholar
  46. Newbold JD, Oneill RV, Elwood JW, Vanwinkle W. 1982. Nutrient spiralling in streams—implications for nutrient limitation and invertebrate activity. American Naturalist 120:628–52.CrossRefGoogle Scholar
  47. Palmer MA, Liermann CAR, Nilsson C, Florke M, Alcamo J, Lake PS, Bond N. 2008. Climate change and the world’s river basins: anticipating management options. Front Ecol Environ 6:81–9.CrossRefGoogle Scholar
  48. Polis GA, Anderson WB, Holt RD. 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316.CrossRefGoogle Scholar
  49. Porter ET, Cornwell JC, Sanford LP. 2004. Effect of oysters Crassostrea virginica and bottom shear velocity on benthic-pelagic coupling and estuarine water quality. Mar Ecol Prog Ser 271:61–75.CrossRefGoogle Scholar
  50. Riley AJ, Dodds WK. 2012. Whole-stream metabolism: strategies for measuring and modeling diel trends of dissolved oxygen. Freshw Sci 32:56–69.CrossRefGoogle Scholar
  51. Rugenski AT, Murria C, Whiles MR. 2012. Tadpoles enhance microbial activity and leaf decomposition in a neotropical headwater stream. Freshw Biol 57:1904–13.CrossRefGoogle Scholar
  52. Rypel AL, Haag WR, Findlay RH. 2008. Validation of annual growth rings in freshwater mussel shells using cross dating. Can J Fish Aquat Sci 65:2224–32.CrossRefGoogle Scholar
  53. Sansom B, Hornbach D, Hove M, Kilgore J. 2013. Effects of flow restoration on mussel growth in a Wild and Scenic North American River. Aquat Biosyst 9:6.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sansom BJ, Atkinson CL, Vaughn CC. 2016. Growth and longevity estimates for mussel populations in three Ouachita Mountain rivers. Freshw Mollusk Biol Conserv 19:19–26.Google Scholar
  55. Schade JD, MacNeill K, Thomas SA, McNeely FC, Welter JR, Hood J, Goodrich M, Power ME, Finlay JC. 2011. The stoichiometry of nitrogen and phosphorus spiralling in heterotrophic and autotrophic streams. Freshw Biol 56:424–36.CrossRefGoogle Scholar
  56. Schmitz OJ, Beckerman AP, O’Brien KM. 1997. Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78:1388–99.CrossRefGoogle Scholar
  57. Schmitz OJ, Hawlena D, Trussell GC. 2010. Predator control of ecosystem nutrient dynamics. Ecol Lett 13:1199–209.CrossRefPubMedGoogle Scholar
  58. Small GE, Helton AM, Kazanci C. 2009. Can consumer stoichiometric regulation control nutrient spiraling in streams? J N Am Benthol Soc 28:747–65.CrossRefGoogle Scholar
  59. Small GE, Pringle CM, Pyron M, Duff JH. 2011. Role of the fish Astyanax aeneus (Characidae) as a keystone nutrient recycler in low-nutrient Neotropical streams. Ecology 92:386–97.CrossRefPubMedGoogle Scholar
  60. Solorzano L, Sharp JH. 1980. Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnol Oceanogr 25:754–7.CrossRefGoogle Scholar
  61. Spooner DE, Vaughn CC. 2006. Context-dependent effects of freshwater mussels on stream benthic communities. Freshw Biol 51:1016–24.CrossRefGoogle Scholar
  62. Spooner DE, Vaughn CC. 2008. A trait-based approach to species’ roles in stream ecosystems: climate change, community structure, and material cycling. Oecologia 158:307–17.CrossRefPubMedGoogle Scholar
  63. Spooner DE, Vaughn CC. 2009. Species richness and temperature influence mussel biomass: a partitioning approach applied to natural communities. Ecology 90:781–90.CrossRefPubMedGoogle Scholar
  64. Spooner DE, Vaughn CC, Galbraith HS. 2012. Species traits and environmental conditions govern the relationship between biodiversity effects across trophic levels. Oecologia 168:533–48.CrossRefPubMedGoogle Scholar
  65. Sterner RW, Elser JJ. 2002. Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton (NJ).: Princeton University Press.Google Scholar
  66. Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM. 2013. Climate change 2013. The physical science basis. Working group I contribution to the fifth assessment report of the intergovernmental panel on climate change-abstract for decision-makers. Groupe d’experts intergouvernemental sur l’evolution du climat/intergovernmental panel on climate change-IPCC, C/O World Meteorological Organization, 7bis Avenue de la Paix, CP 2300 CH-1211 Geneva 2 (Switzerland).Google Scholar
  67. Strayer DL. 2008. Freshwater mussel ecology: a multifactor approach to distribution and abundance. Berkeley (CA): University of California Press.CrossRefGoogle Scholar
  68. Strayer DL. 2013. Understanding how nutrient cycles and freshwater mussels (Unionoida) affect one another. Hydrobiologia 735:277–92.CrossRefGoogle Scholar
  69. 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 54:429–39.CrossRefGoogle Scholar
  70. Strayer DL, Malcom HM. 2007. Shell decay rates of native and alien freshwater bivalves and implications for habitat engineering. Freshw Biol 52:1611–17.CrossRefGoogle Scholar
  71. Taylor BW, Flecker AS, Hall RO. 2006. Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–6.CrossRefPubMedGoogle Scholar
  72. Vanni MJ. 2002. Nutrient cycling by animals in freshwater ecosystems. Annu Rev Ecol Syst 33:341–70.CrossRefGoogle Scholar
  73. Vanni MJ, Boros G, McIntyre PB. 2013. When are fish sources versus sinks of nutrients in lake ecosystems? Ecology 94:2195–206.CrossRefPubMedGoogle Scholar
  74. Vanni MJ, Flecker AS, Hood JM, Headworth JL. 2002. Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes. Ecol Lett 5:285–93.CrossRefGoogle Scholar
  75. 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 5:1291–305.CrossRefPubMedPubMedCentralGoogle Scholar
  76. Vaughn CC, Nichols SJ, Spooner DE. 2008. Community and foodweb ecology of freshwater mussels. J N Am Benthol Soc 27:409–23.CrossRefGoogle Scholar
  77. Vaughn CC, Spooner DE. 2006. Unionid mussels influence macroinvertebrate assemblage structure in streams. J N Am Benthol Soc 25:691–700.CrossRefGoogle Scholar
  78. Vaughn CC, Spooner DE, Galbraith HS. 2007. Context-dependent species identity effects within a functional group of filter-feeding bivalves. Ecology 88:1654–62.CrossRefPubMedGoogle Scholar
  79. Waldbusser GG, Powell EN, Mann R. 2013. Ecosystem effects of shell aggregations and cycling in coastal waters: an example of Chesapeake Bay oyster reefs. Ecology 94:895–903.CrossRefGoogle Scholar
  80. Wesner JS, Billman EJ, Belk MC. 2012. Multiple predators indirectly alter community assembly across ecological boundaries. Ecology 93:1674–82.CrossRefPubMedGoogle Scholar
  81. Whiles MR, Hall RO, Dodds WK, Verburg P, Huryn AD, Pringle CM, Lips KR, Kilham SS, Colon-Gaud C, Rugenski AT, Peterson S, Connelly S. 2013. Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16:146–57.CrossRefGoogle Scholar
  82. Wotton RS, Malmqvist B, Leonardsson K. 2003. Expanding traditional views on suspension feeders—quantifying their role as ecosystem engineers. Oikos 101:441–3.CrossRefGoogle Scholar
  83. Young RG, Huryn AD. 1996. Interannual variation in discharge controls ecosystem metabolism along a grassland river continuum. Can J Fish Aquat Sci 53:2199–211.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Carla L. Atkinson
    • 1
  • Brandon J. Sansom
    • 2
  • Caryn C. Vaughn
    • 3
  • Kenneth J. Forshay
    • 4
  1. 1.Department of Biological SciencesUniversity of AlabamaTuscaloosaUSA
  2. 2.Civil, Structural, and Environmental EngineeringUniversity at BuffaloBuffaloUSA
  3. 3.Oklahoma Biological Survey, Department of Biology and Ecology and Evolutionary Biology Graduate ProgramUniversity of OklahomaNormanUSA
  4. 4.Robert S. Kerr Environmental Research Center, Office of Research and DevelopmentUnited States Environmental Protection AgencyAdaUSA

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