Abstract
Alder (Alnus spp.) and Pacific salmon (Oncorhynchus spp.) provide key nutrient subsidies to freshwater systems. In southwestern Alaska, alder-derived nutrients (ADNs) are increasing as alder cover expands in response to climate warming, while climate change and habitat degradation are reducing marine-derived nutrients (MDNs) in salmon-spawning habitats. To assess the relative influences of ADN and MDN on aquatic microbial community structure and function, we analyzed lake chemistry, bacterial community structure, and microbial metabolism in 13 lakes with varying alder cover and salmon abundance in southwestern Alaska. We conducted bioassays to determine microbial nutrient limitation and physical factors modulating microbial response to nutrient inputs (+N, +P and +NP treatments). Seasonal shifts in bacterial community structure (F = 7.47, P < 0.01) coincided with changes in lake nitrogen (N) and phosphorus (P) concentrations (r2 = 0.19 and 0.16, both P < 0.05), and putrescine degradation (r2 = 0.13, P = 0.06), suggesting the influx and microbial use of MDN. Higher microbial metabolism occurred in summer than spring, coinciding with salmon runs. Increased microbial metabolism occurred in lakes where more salmon spawned. Microbial metabolic activity was unrelated to alder cover, likely because ADN provides less resource diversity than MDN. When nutrients were added to spring samples, there was greater substrate use by microbial communities from lakes with elevated Chl a concentrations and large relative catchment areas (β estimates for all treatments > 0.56, all P < 0.07). Thus, physical watershed and lake features mediate the effects of nutrient subsidies on aquatic microbial metabolic activity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
Raw data were generated at the University of Illinois at Urbana-Champaign. Derived data supporting the findings of and derived code used to analyze the data in this study are available from the corresponding author (DAD) on request.
References
Adams HE, Crump BC, Kling GW (2015) Isolating the effects of storm events on arctic aquatic bacteria: temperature, nutrients, and community composition as controls on bacterial productivity. Front Microbiol 6:1–13. https://doi.org/10.3389/fmicb.2015.00250
Alaska Department of Fish and Game (2002) Spawning ground survey studies in Bristol Bay 1999–2002. Alaska Department of Fish and Game, Dillingham, USA
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
American Public Health Association (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association/American Water Works Association/Water Environment Federation, Washington DC
Belnap J, Welter JR, Grimm NB, Barger N, Ludwig JA (2005) Linkages between microbial and hydrologic processes in arid and semiarid watersheds. Ecology 86:298–307. https://doi.org/10.1890/03-0567
Bergström A, Jonsson A, Jansson M (2008) Phytoplankton responses to nitrogen and phosphorus enrichment in unproductive Swedish lakes along a gradient of atmospheric nitrogen deposition. Aquat Biol 4:55–64. https://doi.org/10.3354/ab00099
Bouchereau A, Guenot P, Larher F (2000) Analysis of amines in plant materials. J Chromatogr B 747:49–67. https://doi.org/10.1016/S0378-4347(00)00286-3
Buchan A, LeCleir GR, Gulvik CA, González JM (2014) Master recyclers: features and functions of bacteria associated with phytoplankton blooms. Nat Rev Microbiol 12:686–698. https://doi.org/10.1038/nrmicro3326
Choi KH, Dobbs FC (1999) Comparison of two kinds of Biolog microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities. J Microbiol Meth 36:203–213. https://doi.org/10.1016/S0167-7012(99)00034-2
Compton JE, Church MR, Larned ST, Hogsett WE (2003) Nitrogen export from forested watersheds in the Oregon coast range: The role of N2-fixing red alder. Ecosystems 6:773–785. https://doi.org/10.1007/s10021-002-0207-4
Collins SF, Baxter CV, Marcarelli AM, Felicetti L, Florin S, Wipfli MS, Servheen G (2020) Reverberating effects of resource exchanges in stream–riparian food webs. Oecologia 192:179–189. https://doi.org/10.1007/s00442-019-04574-y
Cottrell MT, Kirchman DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microb 66:1692–1697. https://doi.org/10.1128/AEM.66.4.1692-1697.2000
Creed IF, Band LE (1998) Export of nitrogen from catchments within a temperate forest: evidence for a unifying mechanism regulated by variable source area dynamics. Water Resour 34:3105–3120. https://doi.org/10.1029/98WR01924
Crump BC, Kling GW, Bahr M, Hobbie JE (2003) Bacterioplankton community shifts in an arctic lake correlate with seasonal changes in organic matter source. Appl Environ Microb 69:2253–2268. https://doi.org/10.1128/AEM.69.4.2253-2268.2003
Danger M, Leflaive J, Oumarou C, Ten-Hage L, Lacroix G (2007a) Control of phytoplankton? Bacteria interactions by stoichiometric constraints. Oikos 116:1079–1086. https://doi.org/10.1111/j.0030-1299.2007.15424.x
Danger M, Oumarou C, Benest D, Lacroix D (2007b) Bacteria can control stoichiometry and nutrient limitation of phytoplankton. Funct Ecol 21:202–210. https://doi.org/10.1111/j.1365-2435.2006.01222.x
Davidson K, Gilpin LC, Hart MC, Fouilland E, Mitchell E, Calleja IA, Laurent C, Miller AEJ, Leakey RJG (2007) The influence of the balance of inorganic and organic nitrogen on the trophic dynamics of microbial food webs. Limnol Oceanogr 52:2147–2163. https://doi.org/10.4319/lo.2007.52.5.2147
Devotta DA (2017) The impacts of alder (Alnus spp.) and salmon (Oncorhynchus spp.) on aquatic nutrient dynamics and microbial communities in southwestern Alaska. PhD dissertation, program in ecology, evolution, and conservation biology, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA
Devotta DA, Fraterrigo JM, Walsh PB, Lowe S, Sewell DK, Schindler DE, Hu FS (2021) Watershed Alnus cover alters N: P stoichiometry and intensifies P limitation in subarctic streams. Biogeochemistry 153:155–176. https://doi.org/10.1007/s10533-021-00776-w
Ebel JD, Leroux SJ, Robertson MJ, Dempson JB (2016) Whole body-element composition of Atlantic salmon Salmo salar influenced by migration direction and life stage in three distinct populations. J Fish Biol 89:2365–2374. https://doi.org/10.1111/jfb.13123
Edmonds RL, Mikkelsen K (2006) Influence of salmon carcass placement in red alder riparian areas on stream chemistry in lowland western Washington. N Am J Fish Manage 26:551–558. https://doi.org/10.1577/M05-095.1
Eilers H, Pernthaler J, Amann R (2000) Succession of pelagic marine bacteria during enrichment: a close look at cultivation-induced shifts. Appl Environ Microb 66:4634–4640. https://doi.org/10.1128/aem.66.11.4634-4640.2000
Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microb 65:4630–4636. https://doi.org/10.1128/AEM.65.10.4630-4636.1999
Garland JL (1996) Analytical approaches to the characterization of samples of microbial communities using patterns of potential C source utilization. Soil Biol Biochem 28:213–221. https://doi.org/10.1016/0038-0717(95)00112-3
Garland JL, Mills AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microb 57:2351–2359. https://doi.org/10.1128/AEM.57.8.2351-2359.1991
Gende SM, Edwards RT, Willson MF, Wipfli MS (2002) Pacific salmon in aquatic and terrestrial ecosystems. Bioscience 52:917. https://doi.org/10.1641/0006-3568(2002)052[0917:PSIAAT]2.0.CO;2
Goldman CR (1961) The contribution of alder trees (Alnus Tenuifolia) to the primary productivity of Castle Lake, California. Ecology 42:282–288. https://doi.org/10.2307/1932080
Holtgrieve GW, Schindler DE (2011) Marine-derived nutrients, bioturbation, and ecosystem metabolism: reconsidering the role of salmon in streams. Ecology 92:373–385. https://doi.org/10.1890/09-1694.1
Hood E, Fellman J, Edwards RT (2007) Salmon influences on dissolved organic matter in a coastal temperate brownwater stream: An application of fluorescence spectroscopy. Limnol Oceanogr 52:1580–1587. https://doi.org/10.4319/lo.2007.52.4.1580
Hu FS, Fraterrigo J, Schindler D, Walsh P, Devotta D, Lowe S, Sands T (2013) Salmon and alder as drivers of nutrient availability and lake productivity in southwestern Alaska. (Final Report) U.S. Fish and Wildlife Service Dillingham, Alaska, USA
Hulot FD, Lacroix G, Lescher-Moutoue F, Loreau M (2000) Functional diversity governs ecosystem response to nutrient enrichment. Nature 405:340–344. https://doi.org/10.1038/35012591
Janetski DJ, Chaloner DT, Tiegs SD, Lamberti GA (2009) Pacific salmon effects on stream ecosystems: a quantitative synthesis. Oecologia 159:583–595. https://doi.org/10.1007/s00442-008-1249-x
Jones LA, Schoen ER, Shaftel R, Cunningham CJ, Mauger S, Rinella DJ, St. Saviour A (2020) Watershed-scale climate influences productivity of Chinook salmon populations across southcentral Alaska. Glob Chang Biol 26:4919–4936. https://doi.org/10.1111/gcb.15155
Jorgensen LV, Huss HH, Dalgaard P (2000) The effect of biogenic amine production by single bacterial cultures and metabiosis on cold-smoked salmon. J Appl Microbiol 89:920–934. https://doi.org/10.1046/j.1365-2672.2000.01196.x
Judd KE, Crump BC, Kling GW (2006) Variation in dissolved organic matter controls bacterial production and community composition. Ecology 87:2068–2079. https://doi.org/10.1890/0012-9658(2006)87[2068:VIDOMC]2.0.CO;2
Kent AD, Yannarell AC, Rusak JA, Triplett EW, McMahon KD (2007) Synchrony in aquatic microbial community dynamics. ISME J 1:38–47. https://doi.org/10.1038/ismej.2007.6
Kõiv T, Nõges T, Laas A (2011) Phosphorus retention as a function of external loading, hydraulic turnover time, area and relative depth in 54 lakes and reservoirs. Hydrobiologia 660:105–115. https://doi.org/10.1007/s10750-010-0411-8
Konopka A, Oliver L, Turco RF Jr (1998) The use of carbon substrate utilization patterns in environmental and ecological microbiology. Microb Ecol 35:103–115. https://doi.org/10.1007/s002489900065
Lachat Instruments (1992) Total Phosphorus in Persulfate Digest. Method Number 10-115-01-1-F, Hach, Milwaukee, Wisconsin, USA
Larsen S, Muehlbauer JD, Marti E (2016) Resource subsidies between stream and terrestrial ecosystems under global change. Glob Change Biol 22:2489–2504. https://doi.org/10.1111/gcb.13182
Leflaive J, Danger M, Lacroix G, Lyautey E, Oumarou C, Ten-Hage L (2008) Nutrient effects on the genetic and functional diversity of aquatic bacterial communities. FEMS Microbiol Ecol 66:379–390. https://doi.org/10.1111/j.1574-6941.2008.00593.x
Lennon JT, Cottingham KL (2008) Microbial productivity in variable resource environments. Ecology 89:1001–1014. https://doi.org/10.1890/07-1380.1
Levine MA, Whalen SC (2001) Nutrient limitation of phytoplankton production in Alaskan Arctic foothill lakes. Hydrobiologia 455:189–201. https://doi.org/10.1023/A:1011954221491
Lowe S, Piazza S, Walsh P (2013) Estimates of surface area and volume for 25 lakes, Togiak National Wildlife Refuge, southwestern Alaska. U.S. Fish and Wildlife Service, Dillingham, Alaska, USA
MacDonald, R (1996) Baseline physical, biological, and chemical parameters of 21 lakes, Togiak National Wildlife Refuge, 1984-1990. U.S. Fish and Wildlife Service, Anchorage, USA
Marks Rupp HS, Anderson CR (2005) Determination of putrescine and cadaverine in seafood (finfish and shellfish) by liquid chromatography using pyrene excimer fluorescence. J Chromatogr A 1094:60–69. https://doi.org/10.1016/j.chroma.2005.07.088
Morris DP, Lewis WM (1988) Phytoplankton nutrient limitation in Colorado mountain lakes. Freshwater Biol 20:315–327. https://doi.org/10.1111/j.1365-2427.1988.tb00457.x
Myers-Smith IH, Forbes BC, Wilmking M, Hallinger M, Lantz T, Blok D, Tape KD, Macias-Fauria M, Sass-Klaassen U, Lévesque E, Boudreau S, Ropars P, Hermanutz L, Trant A, Collier LS, Weijers S, Rozema J, Rayback SA, Schmidt NM, Schaepman-Strub G, Wipf S, Rixen C, Ménard CB, Venn S, Goetz S, Andreu- Hayles L, Elmendorf S, Ravolainen V, Welker J, Grogan P, Epstein HE, Hik DS (2011) Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities. Environ Res Lett 6:45509–45524. https://doi.org/10.1088/1748-9326/6/4/045509
Naiman RJ, Bilby RE, Schindler DE, Helfield JM (2002) Pacific salmon, nutrients, and the dynamics of freshwater and riparian ecosystems. Ecosystems 5:399–417. https://doi.org/10.1007/s10021-001-0083-3
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2016) Vegan: Community Ecology Package. R package version 2.4–1. http://cran.r-project.org/, http://vegan.r-forge.r-project.org
Paerl HW, Dyble J, Moisander PH, Noble RT, Piehler MF, Pinckney JL, Steppe TF, Twomey L, Valdes LM (2003) Microbial indicators of aquatic ecosystem change: current applications to eutrophication studies. FEMS Microbiol Ecol 46:233–246. https://doi.org/10.1016/S0168-6496(03)00200-9
Paver SF, Hayek KR, Gano KA, Fagen JR, Brown CT, Davis-Richardson AG, Crabb DB, Rosario-Passapera R, Giongo A, Triplett EW, Kent AD (2013) Interactions between specific phytoplankton and bacteria affect lake bacterial community succession. Environ Microbiol 15:2489–2504. https://doi.org/10.1111/1462-2920.12131
Pearson RG, Phillips SJ, Loranty MM, Beck PSA, Damoulas T, Knight SJ, Goetz SJ (2013) Shifts in Arctic vegetation and associated feedbacks under climate change. Nat Clim Change 3:673–677. https://doi.org/10.1038/nclimate1858
Preston-Mafham J, Boddy L, Randerson PF (2002) Analysis of microbial community functional diversity using sole-carbon-source utilisation profiles – a critique. FEMS Microbiol Ecol 42:1–14. https://doi.org/10.1111/j.1574-6941.2002.tb00990.x
Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae–bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29. https://doi.org/10.1016/j.biotechadv.2015.12.003
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing
Reisinger AJ, Chaloner DT, Ruegg J, Tiegs SD, Lamberti GA (2013) Effects of spawning Pacific salmon on the isotopic composition of biota differ among southeast Alaska streams. Freshwater Biol 58:938–950. https://doi.org/10.1111/fwb.12098
Ruckelshaus MH, Levin P, Johnson JB, Kareiva PM (2002) The Pacific salmon wars: What science brings to the challenge of recovering species. Annu Rev Ecol Syst 33:665–706. https://doi.org/10.1146/annurev.ecolsys.33.010802.150504
Ruiz-González C, Niño-García JP, Lapierre JF, del Giorgio PA (2015) The quality of organic matter shapes the functional biogeography of bacterioplankton across boreal freshwater ecosystems. Global Ecol and Biogeogr 24:1487–1498. https://doi.org/10.1111/geb.12356
Salmon VG, Breen AL, Kumar J, Mara MJ, Thornton PE, Wullschleger SD, Iversen CM (2019) Alder distribution and expansion across a tundra hillslope: implications for local N cycling. Front Plant Sci 10:1099. https://doi.org/10.3389/fpls.2019.01099
Sarmento H, Montoya JM, Vazquez-Dominguez E, Vaque D, Gasol JM (2010) Warming effects on marine microbial food web processes: how far can we go when it comes to predictions? Philos T R Soc b: Biological Sciences 365:2137–2149. https://doi.org/10.1098/rstb.2010.0045
Schaefer SC, Hollibaugh JT, Alber M (2009) Watershed nitrogen input and riverine export on the west coast of the US. Biogeochemistry 93:219–233. https://doi.org/10.1007/s10533-009-9299-7
Schindler DE, Leavitt PR, Brock CS, Johnson SP, Quay PD (2005) Marine-derived nutrients, commercial fisheries, and production of salmon and lake algae in Alaska. Ecology 86:3225–3231. https://doi.org/10.1890/04-1730
Schindler DE, Scheuerell MD, Moore JW, Gende SM, Francis TB, Palen WJ (2003) Pacific salmon and the ecology of coastal ecosystems. Front Ecol Environ 1:31–37. https://doi.org/10.1890/1540-9295(2003)001[0031:PSATEO]2.0.CO;2
Morris A, Meyer K, Bohannan B (2020) Linking microbial communities to ecosystem functions: What we can learn from genotype-phenotype mapping in organisms. Philos Trans R Soc Lond B Biol Sci 375:20190244. https://doi.org/10.1098/rstb.2019.0244
Tape KD, Hallinger M, Welker JM, Ruess RW (2012) Landscape heterogeneity of shrub expansion in Arctic Alaska. Ecosystems 15:711–724. https://doi.org/10.1007/s10021-012-9540-4
Tape K, Sturm M, Racine C (2006) The evidence for shrub expansion in Northern Alaska and the Pan-Arctic. Glob Change Biol 12:686–702. https://doi.org/10.1111/j.1365-2486.2006.01128.x
Tundisi JG, Straškraba M (1999) Theoretical reservoir ecology and its applications. International Institute of Ecology. Backhuys Publishers, Netherlands
Vanni MJ, Boros G, McIntyre PB (2013) When are fish sources v. sinks of nutrients in lake ecosystems? Ecology 94:2195–2206. https://doi.org/10.1890/12-1559.1
Vallières C, Retamal L, Ramlal P, Osburn CL, Vincent WF (2008) Bacterial production and microbial food web structure in a large arctic river and the coastal Arctic Ocean. J Marine Syst 74:756–773. https://doi.org/10.1016/j.jmarsys.2007.12.002
Vinagre J, Rodríguez A, Larraín MA, Aubourg SP (2011) Chemical composition and quality loss during technological treatment in coho salmon (Oncorhynchus kisutch). Food Res Int 44:1–13. https://doi.org/10.1016/j.foodres.2010.10.040
Wang T, Hung CCY, Randall DJ (2006) The comparative physiology of food deprivation: from feast to famine. Annu Rev Physiol 68:223–251. https://doi.org/10.1146/annurev.physiol.68.040104.105739
Walker CM, King RS, Whigham DF, Baird SJ (2012) Landscape and wetland influences on headwater stream chemistry in the Kenai Lowlands, Alaska. Wetlands 32:301–310. https://doi.org/10.1007/s13157-011-0260-x
Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992. https://doi.org/10.4319/lo.1994.39.8.1985
Whalen SC, Cornwell JC (1985) Nitrogen, phosphorus, and organic carbon cycling in an Arctic lake. Can J Fish Aquat Sci 42:797–808. https://doi.org/10.1139/f85-102
Wood ED, Armstrong FAJ, Richards FA (1967) Determination of nitrate in sea water by cadmium-copper reduction to nitrite. J Mar Biol Assoc UK 47:23–31. https://doi.org/10.1017/S002531540003352X
Wrona FJ, Johansson M, Culp JM, Jenkins A, Mård J, Myers-Smith IH, Prowse TD, Vincent WF, Wookey PA (2016) Transitions in Arctic ecosystems: Ecological implications of a changing hydrological regime. J Geophys Res-Biogeo 121:650–674. https://doi.org/10.1002/2015JG003133
Yoder DM, Viramontes A, Kirk LL, Hanne LF (2011) Impact of salmon spawning on microbial communities in a northern California river. J Freshwater Ecol 21:147–155. https://doi.org/10.1080/02705060.2006.9664107
Acknowledgements
Funding for this research was provided by the U.S. Fish and Wildlife Service and the University of Illinois at Urbana-Champaign. We thank ADK’s students who provided input on the study design and helped analyze the samples and the TNWR staff who helped collect the samples. We especially thank Tim Sands, the experienced fish biologist from the Alaska Department of Fish and Game who conducted the aerial salmon surveys. Also, we are grateful to Anthony C. Yannarell for use of his lab to incubate and analyze the Biolog plates and Mario E. Muscarella who provided feedback on data analyses.
Funding
Funding for this research was provided by the U.S. Fish and Wildlife Service and the University of Illinois at Urbana-Champaign.
Author information
Authors and Affiliations
Contributions
DAD, FSH and ADK conceived the study, DAD and PBW collected the samples, DAD and ADK analyzed the samples, DAD and DMN led manuscript development, and all authors contributed to writing. All authors confirm this manuscript has not been published elsewhere, is original, and is not under consideration by another journal. All authors agree to be listed and approve the submitted version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
None of the authors have any conflicts of interest to declare.
Ethics approval
Ethics approval was not required for this study as no humans or animals were involved.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Communicated by Carla Atkinson.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Devotta, D.A., Kent, A.D., Nelson, D.M. et al. Effects of alder- and salmon-derived nutrients on aquatic bacterial community structure and microbial community metabolism in subarctic lakes. Oecologia 199, 711–724 (2022). https://doi.org/10.1007/s00442-022-05207-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-022-05207-7