Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-28T05:00:07.409Z Has data issue: false hasContentIssue false

Young, Old, and Weathered Carbon—Part 2: Using Radiocarbon and Stable Isotopes to Identify Terrestrial Carbon Support of the Food Web in an Alkaline, Humic Lake

Published online by Cambridge University Press:  09 February 2016

Evelyn M Keaveney*
Affiliation:
14CHRONO Centre, School of Geography, Archaeology and Palaeoecology, Queen's University Belfast BT71NN, UK
Paula J Reimer
Affiliation:
14CHRONO Centre, School of Geography, Archaeology and Palaeoecology, Queen's University Belfast BT71NN, UK
Robert H Foy
Affiliation:
Agri-Food and Biosciences Institute, Newforge Lane, Belfast BT95PX, UK School of Biological Sciences, Queen's University Belfast BT71NN, UK
*
2.Corresponding author. Email: e.keaveney@qub.ac.uk.

Abstract

Carbon (C) and nitrogen (N) stable isotope analysis (SIA) has been used to identify the terrestrial subsidy of freshwater food webs. However, SIA fails to differentiate between the contributions of old and recently fixed terrestrial C and consequently cannot fully determine the source, age, and biochemical quality of terrestrial carbon. Natural abundance radiocarbon (Δ14C) was used to examine the age and origin of carbon in Lower Lough Erne, Northern Ireland. 14C and stable isotope values were obtained from invertebrate, algae, and fish samples, and the results indicate that terrestrial organic C is evident at all trophic levels. High winter δ15N values in calanoid zooplankton (δ15N = 24‰) relative to phytoplankton and particulate organic matter (δ15N = 6‰ and 12‰, respectively) may reflect several microbial trophic levels between terrestrial C and calanoid invertebrates. Winter and summer calanoid Δ14C values show a seasonal switch between autochthonous and terrestrial carbon sources. Fish Δ14C values indicate terrestrial support at the highest trophic levels in littoral and pelagic food webs. 14C therefore is useful in attributing the source of carbon in freshwater in addition to tracing the pathway of terrestrial carbon through the food web.

Type
Articles
Copyright
Copyright © 2015 by the Arizona Board of Regents on behalf of the University of Arizona 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ågren, A, Berggren, M, Laudon, H, Jansson, M. 2008. Terrestrial export of highly bioavailable carbon from small boreal catchments in spring floods. Freshwater Biology 53(5):964–72.Google Scholar
Ascough, PL, Cook, GT, Church, MJ, Dugmore, AJ, McGovern, T, Dunbar, E, Einarsson, E, Fri∂riksson, A, Gestsdottir, H. 2007. Reservoirs and radiocarbon: 14C dating problems in Mývatnssveit, northern Iceland. Radiocarbon 49(2):947–61.Google Scholar
Ascough, P, Cook, G, Church, M, Dunbar, E, Einarsson, Á, McGovern, T, Dugmore, A, Perdikaris, S, Hastie, H, Fri∂riksson, A. 2010. Temporal and spatial variations in freshwater 14C reservoir effects: Lake Mývatn, northern Iceland. Radiocarbon 52(2–3):1098–112.CrossRefGoogle Scholar
Battarbee, RW. 1986. The eutrophication of Lough Erne inferred from changes in the diatom assemblages of 210Pb- and 37Cs-dated sediment cores. Proceedings of the Royal Irish Academy 86B:141–68.Google Scholar
Billett, MF, Garnett, MH, Dinsmore, KJ, Dyson, KE, Harvey, F, Thomson, AM, Piirainen, S, Kortelainen, P. 2012. Age and source of different forms of carbon released from boreal peatland streams during spring snowmelt in E. Finland. Biogeochemistry 111(1–3):273–86.Google Scholar
Bond, AL, Diamond, AW. 2011. Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecological Applications 21(4):1017–23.CrossRefGoogle ScholarPubMed
Broecker, WS, Orr, PC. 1958. Radiocarbon chronology of Lake Lahontan and Lake Bonneville. Geological Society of America Bulletin 69(8):1009–32.Google Scholar
Broecker, WS, Walton, A. 1959. The geochemistry of C 14 in fresh-water systems. Geochimica et Cosmochimica Acta 16(1–3):1538.CrossRefGoogle Scholar
Butman, D, Raymond, PA, Butler, K, Aiken, G. 2012. Relationships between Δ14C and the molecular quality of dissolved organic carbon in rivers draining to the coast from the conterminous United States. Global Biogeochemical Cycles 26(4):GB4014, doi:10.1029/2012GB004361.Google Scholar
Caraco, N, Bauer, JE, Cole, JJ, Petsch, S, Raymond, P. 2010. Millennial-aged organic carbon subsidies to a modern river food web. Ecology 91(8):2385–93.Google Scholar
Carpenter, SR, Cole, JJ, Pace, ML, Van de Bogert, M, Bade, DL, Bastviken, D, Gille, CM, Hodgson, JR, Kitchell, JF, Kritzberg, ES. 2005. Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86(10):2737–50.Google Scholar
Caut, S, Angulo, E, Courchamp, F. 2009. Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46(2):443–53.CrossRefGoogle Scholar
Cole, JJ, Carpenter, SR, Kitchell, J, Pace, ML, Solomon, CT, Weidel, B. 2011. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Proceedings of the National Academy of Sciences of the USA 108(5):1975–80.Google Scholar
de Kluijver, A, Yu, J, Houtekamer, M, Middelburg, JJ, Liu, Z. 2012. Cyanobacteria as carbon source for zooplankton in eutrophic Lake Taihu, China, measured by 13C labelling and fatty acid biomarkers. Limnology and Oceanography 57(4):1245–54.CrossRefGoogle Scholar
Deevey, ES, Gross, MS, Hutchinson, GE, Kraybill, HL. 1954. The natural C14 contents of materials from hard-water lakes. Proceedings of the National Academy of Sciences of the USA 40(5):285–8.Google Scholar
Foy, RH, McGlynn, K, Gibson, CE. 1993. Chlorophyll a and nutrients in Lough Erne. Biology and Environment: Proceedings of the Royal Irish Academy 93B(3):163–74.Google Scholar
Fry, B. 1991. Stable isotope diagrams of freshwater food webs. Ecology 72(6):2293–7.CrossRefGoogle Scholar
Garnett, M, Hardie, S, Murray, C, Billett, M. 2013. Radiocarbon dating of methane and carbon dioxide evaded from a temperate peatland stream. Biogeochemistry 114(1–3):213–23.CrossRefGoogle Scholar
Ger, KA, Panosso, R, Luerling, M. 2011. Consequences of acclimation to Microcystis on the selective feeding behavior of the calanoid copepod Eudiaptomus gracilis . Limnology and Oceanography 56(6):2103–14.Google Scholar
Gibson, C, Foy, R, Fitzsimons, A. 1980. A limnological reconnaissance of the Lough Erne system, Ireland. Internationale Revue der Gesamten Hydrobiologie und Hydrographie 65(1):4984.Google Scholar
Gibson, C, McCall, R, Dymond, A. 1993. Skeletonema subsalsum in a freshwater Irish lake. Diatom Research 8(1):6571.Google Scholar
Gibson, C, Anderson, N, Zhou, Q, Allen, M, Appleby, P. 2003. Changes in sediment and diatom deposition in Lower Lough Erne c. 1920–90. Biology and Environment: Proceedings of the Royal Irish Academy 103B(1):31–9.Google Scholar
Gibson, C, Foy, R, McNally, J. 2005. Stratification and oxygen depletion in Lower Lough Erne 1991–2000. Biology and Environment: Proceedings of the Royal Irish Academy 105B(2):81–6.Google Scholar
Ginestet, C. 2011. ggplot2: elegant graphics for data analysis. Journal of the Royal Statistical Society: Series A 174(1):245–6.Google Scholar
Gratton, C, Donaldson, J, Zanden, M. 2008. Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11(5):764–74.Google Scholar
Grey, JJ, Jones, RI, Sleep, D. 2001. Seasonal changes in the importance of the source of organic matter to the diet of zooplankton in Loch Ness, as indicated by stable isotope analysis. Limnology and Oceanography 46(3):505–13.Google Scholar
Guillemette, F, McCallister, SL, Giorgio, PA. 2013. Differentiating the degradation dynamics of algal and terrestrial carbon within complex natural dissolved organic carbon in temperate lakes. Journal of Geophysical Research: Biogeosciences 118(3):963–73.Google Scholar
Guo, L, Ping, C-L, Macdonald, RW. 2007. Mobilization pathways of organic carbon from permafrost to arctic rivers in a changing climate. Geophysical Research Letters 34(13):L13603.Google Scholar
Hamilton, SK, Sippel, SJ, Bunn, SE. 2005. Separation of algae from detritus for stable isotope or ecological stoichiometry studies using density fractionation in colloidal silica. Limnology and Oceanography: Methods 3:149–57.Google Scholar
Harrell, FE Jr, Dupont, MC, Hmisc, D. 2007. The design package. R package version: 2.1. http://cran.r-project.org.Google Scholar
Harrod, C, Griffiths, D, McCarthy, T, Rosell, R. 2001. The Irish pollan, Coregonus autumnalis: options for its conservation. Journal of Fish Biology 59(sA):339–55.Google Scholar
Hua, Q, Barbetti, M. 2004. Review of tropospheric bomb 14C data for carbon cycle modeling and age calibration purposes. Radiocarbon 46(3):1273–98.Google Scholar
Jensen, H, Kiljunen, M, Amundsen, PA. 2012. Dietary ontogeny and niche shift to piscivory in lacustrine brown trout Salmo trutta revealed by stomach content and stable isotope analyses. Journal of Fish Biology 80(7):2448–62.CrossRefGoogle ScholarPubMed
Keaveney, EM, Reimer, PJ. 2012. Understanding the variability in freshwater radiocarbon reservoir offsets: a cautionary tale. Journal of Archaeological Science 39(5):1306–16.Google Scholar
Keaveney, EM, Reimer, PJ, Foy, RH. 2015. Young, old, and weathered carbon—Part 1: using radiocarbon and stable isotopes to identify carbon sources in an alkaline, humic lake. Radiocarbon 57(3):407–23. [this issue].Google Scholar
Kritzberg, ES, Cole, JJ, Pace, MM, Granéli, W. 2006a. Bacterial growth on allochthonous carbon in humic and nutrient-enriched lakes: results from whole-lake 13C addition experiments. Ecosystems 9(3):489–99.Google Scholar
Kritzberg, ES, Langenheder, S, Lindström, ES. 2006b. Influence of dissolved organic matter source on lake bacterioplankton structure and function–implications for seasonal dynamics of community composition. FEMS Microbiology Ecology 56(3):406–17.Google Scholar
Lapierre, J-F, Guillemette, F, Berggren, M, del Giorgio, PA. 2013. Increases in terrestrially derived carbon stimulate organic carbon processing and CO2 emissions in boreal aquatic ecosystems. Nature Communications 4:2972.Google Scholar
Layman, CA, Araujo, MS, Boucek, R, Hammerschlag-Peyer, CM, Harrison, E, Jud, ZR, Matich, P, Rosenblatt, AE, Vaudo, JJ, Yeager, LA. 2012. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews 87(3):545–62.Google Scholar
Levin, I, Kromer, B. 2004. The tropospheric 14CO2 level in mid latitudes of the northern hemisphere (1959–2003). Radiocarbon 46(3):1261–71.CrossRefGoogle Scholar
Levin, I, Hammer, S, Kromer, B, Meinhardt, F. 2008. Radiocarbon observations in atmospheric CO2: determining fossil fuel CO2 over Europe using Jungfraujoch observations as background. Science of the Total Environment 391(2):211–6.CrossRefGoogle ScholarPubMed
Levin, I, Kromer, B, Hammer, S. 2013. Atmospheric Δ14CO2 trend in Western European background air from 2000 to 2012. Tellus B 65:20092.Google Scholar
Maguire, C, Gibson, C. 2005. Ecological change in Lough Erne: influence of catchment changes and species invasions. Freshwater Forum 24(1):3858.Google Scholar
Maguire, CM, Grey, J. 2006. Determination of zooplankton dietary shift following a zebra mussel invasion, as indicated by stable isotope analysis. Freshwater Biology 51(7):1310–9.Google Scholar
Marty, J, Planas, D. 2008. Comparison of methods to determine algal δ13C in freshwater. Limnology and Oceanography: Methods 6(1):5163.Google Scholar
McCallister, SL, del Giorgio, PA. 2008. Direct measurement of the δ13C signature of carbon respired by bacteria in lakes: linkages to potential carbon sources, ecosystem baseline metabolism, and CO2 fluxes. Limnology and Oceanography 53(4):1204–16.Google Scholar
Meyer, J. 1994. The microbial loop in flowing waters. Microbial Ecology 28(2):195–9.Google Scholar
Neff, J, Finlay, J, Zimov, S, Davydov, S, Carrasco, J, Schuur, E, Davydova, A. 2006. Seasonal changes in the age and structure of dissolved organic carbon in Siberian rivers and streams. Geophysical Research Letters 33:L23401, doi:10.1029/2006GL028222.Google Scholar
Parnell, A, Inger, R, Bearhop, S, Jackson, A. 2008. SIAR: stable isotope analysis in R. The Comprehensive R Archive Network. Available at http://cran.r-project.org/web/packages/siar/index.html. Accessed 15 July 2012.Google Scholar
Pasche, N, Schmid, M, Vazquez, F, Schubert, CJ, Wüest, A, Kessler, JD, Pack, MA, Reeburgh, WS, Bürgmann, H. 2011. Methane sources and sinks in Lake Kivu. Journal of Geophysical Research: Biogeosciences 116(G3):G03006.Google Scholar
Perga, M-E, Gerdeaux, D. 2004. Changes in the δ13C of pelagic food webs: the influence of lake area and trophic status on the isotopic signature of whitefish (Coregonus lavaretus). Canadian Journal of Fisheries and Aquatic Sciences 61(8):1485–92.Google Scholar
Phillips, DL, Inger, R, Bearhop, S, Jackson, AL, Moore, JW, Parnell, AC, Semmens, BX, Ward, EJ. 2014. Best practices for use of stable isotope mixing models in food-web studies. Canadian Journal of Zoology 92(10):823–35.Google Scholar
Polsenaere, P, Savoye, N, Etcheber, H, Canton, M, Poirier, D, Bouillon, S, Abril, G. 2013. Export and degassing of terrestrial carbon through watercourses draining a temperate podzolized catchment. Aquatic Sciences 75(2):299319.Google Scholar
Rautio, M, Vincent, FW. 2007. Isotopic analysis of the sources of organic carbon for zooplankton in shallow subarctic and arctic waters. Ecography 30(1):7787.Google Scholar
Rautio, M, Mariash, H, Forsström, L. 2011. Seasonal shifts between autochthonous and allochthonous carbon contributions to zooplankton diets in a subarctic lake. Limnology and Oceanography 56(4):1513–24.Google Scholar
Raymond, PA, McClelland, J, Holmes, R, Zhulidov, A, Mull, K, Peterson, B, Striegl, R, Aiken, G, Gurtovaya, T. 2007. Flux and age of dissolved organic carbon exported to the Arctic Ocean: a carbon isotopic study of the five largest arctic rivers. Global Biogeochemical Cycles 21:GB4011, doi:10.1029/2007GB002934.CrossRefGoogle Scholar
Raymond, PA, Hartmann, J, Lauerwald, R, Sobek, S, McDonald, C, Hoover, M, Butman, D, Striegl, R, Mayorga, E, Humborg, C. 2013. Global carbon dioxide emissions from inland waters. Nature 503(7476):355–9.CrossRefGoogle ScholarPubMed
Reimer, PJ, Brown, TA, Reimer, RW. 2004. Discussion: reporting and calibration of post-bomb 14C data. Radiocarbon 46(3):1299–304.Google Scholar
Rosell, R, Gibson, C. 2000. Interlinked changes in fish populations and their environments in lower Lough Erne, Northern Ireland. Verhandlungen der Internationale Verein für Limnologie 27:2095–9.Google Scholar
Rosell, R, Maguire, C, McCarthy, T. 1998. First reported settlement of zebra mussels Dreissena polymorpha in the Erne System, Co. Fermanagh, Northern Ireland. Biology and Environment: Proceedings of the Royal Irish Academy 98B(3):191–3.Google Scholar
Rottberger, J, Gruber, A, Boenigk, J, Kroth, PG. 2013. Influence of nutrients and light on autotrophic, mixotrophic and heterotrophic freshwater chrysophytes. Aquatic Microbial Ecology 71(2):179–91.Google Scholar
Seifert, LI, Scheu, S. 2012. Linking aquatic and terrestrial food webs–Odonata in boreal systems. Freshwater Biology 57(7):1449–57.Google Scholar
Smyntek, PM, Maberly, SC, Grey, J. 2012. Dissolved carbon dioxide concentration controls baseline stable carbon isotope signatures of a lake food web. Limnology and Oceanography 57(5):1292–302.Google Scholar
Stuiver, M, Polach, HA. 1977. Discussion: reporting of 14C data. Radiocarbon 19(3):355–63.Google Scholar
Taipale, S, Kankaala, P, Jones, RI. 2007. Contributions of different organic carbon sources to Daphnia in the pelagic foodweb of a small polyhumic lake: results from mesocosm DI13C-additions. Ecosystems 10(5):757–72.Google Scholar
Taipale, S, Kankaala, P, Tiirola, M, Jones, RI. 2008. Whole-lake dissolved inorganic 13C additions reveal seasonal shifts in zooplankton diet. Ecology 89(2):463–74.Google Scholar
Tittel, J, Wiehle, I, Wannicke, N, Kampe, H, Poerschmann, J, Meier, J, Kamjunke, N. 2009. Utilisation of terrestrial carbon by osmotrophic algae. Aquatic Sciences 71(1):4654.CrossRefGoogle Scholar
Trumbore, S. 2009. Radiocarbon and soil carbon dynamics. Annual Review of Earth and Planetary Sciences 37:4766.Google Scholar
Trumbore, S, Vogel, J, Southon, J. 1989. AMS 14C measurements of fractionated soil organic matter: an approach to deciphering the soil carbon cycle. Radiocarbon 31(3):644–54.Google Scholar
van der Plicht, J, Hogg, A. 2006. A note on reporting radiocarbon. Quaternary Geochronology 1(4):23740.Google Scholar
Wilkinson, GM, Pace, ML, Cole, JJ. 2013a. Terrestrial dominance of organic matter in north temperate lakes. Global Biogeochemical Cycles 27(1):4351.Google Scholar
Wilkinson, GM, Carpenter, SR, Cole, JJ, Pace, ML, Yang, C. 2013b. Terrestrial support of pelagic consumers: patterns and variability revealed by a multilake study. Freshwater Biology 58(10):2037–49.Google Scholar
Zhou, Q, Gibson, CE, Foy, RH. 2000. Long-term changes of nitrogen and phosphorus loadings to a large lake in North-West Ireland. Water Research 34(3):922–6.Google Scholar
Zigah, P, Minor, E, Werne, J, McCallister, SL. 2012. An isotopic (14C, δ13C, and δ15N) investigation of the composition of particulate organic matter and zooplankton food sources in Lake Superior and across a size-gradient of aquatic systems. Biogeosciences 9:3663–78.Google Scholar