Skip to main content
SpringerLink
Log in

Seasonality of cladoceran and bryozoan resting stage δ13C values and implications for their use as palaeolimnological indicators of lacustrine carbon cycle dynamics

  • Original paper
  • Published:
Journal of Paleolimnology Aims and scope Submit manuscript

Abstract

The stable carbon isotope composition, expressed as δ13C values, of chitinous resting stages of planktivorous invertebrates can provide information on past changes in carbon cycling in lakes. For example, the δ13C values of cladoceran ephippia and bryozoan statoblasts have been used to estimate the past contribution of methane-derived carbon to lake food webs and variations in the δ13C value of planktonic algae. Limited information, however, is available concerning seasonal variations in δ13C values of these organisms and their resting stages. We measured the seasonal variation in δ13C values of Daphnia (Branchiopoda: Cladocera: Daphniidae) and their floating ephippia over a 2-year period in small, dimictic Lake Gerzensee, Switzerland. Floating ephippia of Ceriodaphnia (Branchiopoda: Cladocera: Daphniidae) and statoblasts of Plumatella (Phylactolaemata: Plumatellida: Plumatellidae) were analysed during parts of this period. Furthermore, δ13C values of remains from all three organism groups were analysed in a 62-cm-long sediment core. Throughout the year, Daphnia δ13C values tracked the δ13C values of particulate organic matter (POM), but were more negative than POM, indicating that Daphnia also utilize a relatively 13C-depleted carbon source. Daphnia ephippia δ13C values did not show any pronounced seasonal variation, suggesting that they are produced batch-wise in autumn and/or spring and float for several months. In contrast, δ13C values of Ceriodaphnia ephippia and Plumatella statoblasts followed variations in δ13CPOM values, Ceriodaphnia values being the most negative of the resting stages. Average cladoceran ephippia δ13C values in the flotsam agreed well with ephippia values from Gerzensee surface sediments. In contrast, average Plumatella statoblast δ13C values from the flotsam were 4‰ more negative than in the surface sediments. In the sediment core, δ13C values of the two cladocerans remained low (mean −39.0 and −41.9‰) throughout the record. In contrast, Plumatella had distinctly less negative δ13C values (mean −32.0‰). Our results indicate that in Gerzensee, Daphnia and Ceriodaphnia strongly relied on a 13C-depleted food source throughout the past 150 years, most likely methane-oxidising bacteria, whereas this food source was not a major contribution to the diet of bryozoans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Albrecht A, Reiser R, Lück A, Stoll J-MA, Giger W (1998) Radiocesium dating of sediments from lakes and reservoirs of different hydrological regimes. Environ Sci Technol 32:1882–1887

    Article  Google Scholar 

  • Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments, vol 1. Basin analysis, coring, and chronological techniques, Kluwer Academic Publishers, Dordrecht, pp 171–203

    Chapter  Google Scholar 

  • Appleby PG, Oldfield F (1978) The calculation of lead-210 dates assuming a constant rate of supply of unsupported 210Pb to the sediment. Catena 5:1–8

    Article  Google Scholar 

  • Bastviken D, Ejlertsson J, Sundh I, Tranvik LJ (2003) Methane as a source of carbon and energy for lake pelagic food webs. Ecology 84:969–981

    Article  Google Scholar 

  • Belle S, Parent C, Frossard V, Verneaux V, Millet L, Chronopoulou P-M, Sabatier P, Magny M (2014) Temporal changes in the contribution of methane-oxidizing bacteria to the biomass of chironomid larvae determined using stable carbon isotopes and ancient DNA. J Paleolimnol 52:215–228

    Article  Google Scholar 

  • Bundesamt für Meteorologie und Klimatologie MeteoSchweiz (2014) Homogene Monatsdaten. Available at: http://www.meteoschweiz.admin.ch/home/klima/vergangenheit/homogene-monatsdaten.html (2015)

  • Bunn SE, Boon PI (1993) What sources of organic carbon drive food webs in billabongs? A study based on stable isotope analysis. Oecologia 96:85–94

    Article  Google Scholar 

  • Cáceres CE (1998) Interspecific variation in the abundance, production, and emergence of Daphnia diapausing eggs. Ecology 79:1699–1710

    Article  Google Scholar 

  • Del Giorgio PA, France RL (1996) Ecosystem-specific patterns in the relationship between zooplankton and POM or microplankton δ13C. Limnol Oceanogr 41:359–365

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  Google Scholar 

  • Devlin SP, Saarenheimo J, Syväranta J, Jones RI (2015) Top consumer abundance influences lake methane efflux. Nat Commun 6:8787

    Article  Google Scholar 

  • EAWAG (1995) Protokoll zur Bestimmung von Chlorophyll a mit Photometrie. Swiss Federal Institute of Aquatic Science and Technology (EAWAG), Dübendorf

  • Edmondson WT (1957) Trophic relations of the zooplankton. Trans Am Microsc Soc 76:225–245

    Article  Google Scholar 

  • France RL (1995) Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnol Oceanogr 40:1310–1313

    Article  Google Scholar 

  • Francis DR (2001) Bryozoan statoblasts. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments, vol 4. Zoological indicators, Kluwer Academic Publishers, Dordrecht, pp 105–123

    Chapter  Google Scholar 

  • Frossard V, Verneaux V, Millet L, Jenny J-P, Arnaud F, Magny M, Perga M-E (2014) Reconstructing long-term changes (150 years) in the carbon cycle of a clear-water lake based on the stable carbon isotope composition (δ13C) of chironomid and cladoceran subfossil remains. Freshw Biol 59:789–802

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • Geller W, Müller H (1981) The filtration apparatus of Cladocera: filter mesh-sizes and their implications on food selectivity. Oecologia 49:316–321

    Article  Google Scholar 

  • Grey J (2016) The incredible lightness of being methane-fuelled: stable isotopes reveal alternative energy pathways in aquatic ecosystems and beyond. Front Ecol Evol 4(8):1–14

    Google Scholar 

  • Heiri O, Schilder J, van Hardenbroek M (2012) Stable isotopic analysis of fossil chironomids as an approach to environmental reconstruction: state of development and future challenges. Fauna Nor 31:7–18

    Google Scholar 

  • Jones RI, Grey J (2011) Biogenic methane in freshwater food webs. Freshw Biol 56:213–229

    Article  Google Scholar 

  • Jones RI, Grey J, Sleep D, Arvola L (1999) Stable isotope analysis of zooplankton carbon nutrition in humic lakes. Oikos 86:97–104

    Article  Google Scholar 

  • Kaminski M (1984) Food composition of three bryozoan species (Bryozoa, Phylactolaemata) in a mesotrophic lake. Pol Arch Hydrobiol 31:45–53

    Google Scholar 

  • Kankaala P, Taipale S, Grey J, Sonninen E, Arvola L, Jones RI (2006) Experimental δ13C evidence for a contribution of methane to pelagic food webs in lakes. Limnol Oceanogr 51:2821–2827

    Article  Google Scholar 

  • Korhola A, Rautio M (2001) Cladocera and other branchiopod crustaceans. In: Smol JP, Birks HJB, Last WM (eds) Tracking environmental change using lake sediments, vol 4, Zoological indicators. Kluwer Academic Publishers, Dordrecht, pp 5–41

    Chapter  Google Scholar 

  • Lampert W (2011) Daphnia: development of a model organism in ecology and evolution. International Ecology Institute, Oldendorf/Luhe

    Google Scholar 

  • Lotter AF, Sturm M, Teranes JL, Wehrli B (1997) Varve formation since 1885 and high-resolution varve analyses in hypertrophic Baldeggersee (Switzerland). Aquat Sci 59:304–325

    Article  Google Scholar 

  • Lotter AF, Birks HJB, Eicher U, Hofmann W, Schwander J, Wick L (2000) Younger Dryas and Allerød summer temperatures at Gerzensee (Switzerland) inferred from fossil pollen and cladoceran assemblages. Palaeogeogr Palaeoclimatol Palaeoecol 159:349–361

    Article  Google Scholar 

  • Matthews B, Mazumder A (2005) Temporal variation in body composition (C:N) helps explain seasonal patterns of zooplankton δ13C. Freshw Biol 50:502–515

    Article  Google Scholar 

  • Okamura B, Hatton-Ellis T (1995) Population biology of bryozoans: correlates of sessile, colonial life histories in freshwater habitats. Experientia 51:510–525

    Article  Google Scholar 

  • Perga M-E (2009) Potential of δ13C and δ15N of cladoceran subfossil exoskeletons for paleo-ecological studies. J Paleolimnol 44:387–395

    Article  Google Scholar 

  • Perga M-E (2011) Taphonomic and early diagenetic effects on the C and N stable isotope composition of cladoceran remains: implications for paleoecological studies. J Paleolimnol 46:203–213

    Article  Google Scholar 

  • Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320

    Article  Google Scholar 

  • R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.r-project.org

  • Rinta P, Bastviken D, van Hardenbroek M, Kankaala P, Leuenberger M, Schilder J, Stötter T, Heiri O (2015) An inter-regional assessment of concentrations and δ13C values of methane and dissolved inorganic carbon in small European lakes. Aquat Sci 77:667–680

    Article  Google Scholar 

  • Rinta P, van Hardenbroek M, Jones RI, Kankaala P, Rey F, Szidat S, Wooller MJ, Heiri O (2016) Land use affects carbon sources to the pelagic food web in a small boreal lake. PLoS ONE 11(8):e0159900

    Article  Google Scholar 

  • Sartory DP, Grobbelaar JU (1984) Extraction of chlorophyll a from freshwater phytoplankton for spectrophotometric analysis. Hydrobiologia 14:177–187

    Article  Google Scholar 

  • Schilder J (2014) Methanogenic carbon in Daphnia tissue as an indicator of lacustrine methane budgets. Observations from the field, experiments and fossil records. Ph.D.-Thesis, University of Bern

  • Schilder J, Bastviken D, van Hardenbroek M, Leuenberger M, Rinta P, Stötter T, Heiri O (2015a) The δ13C values of Daphnia ephippia reflect in-lake methane availability. Limnol Oceanogr 60:1064–1075

    Article  Google Scholar 

  • Schilder J, Tellenbach C, Möst M, Spaak P, van Hardenbroek M, Wooller M, Heiri O (2015b) The stable isotopic composition of Daphnia ephippia reflects changes in δ13C and δ18O values of food and water. Biogeosciences 12:3819–3830

    Article  Google Scholar 

  • Schilder J, Bastviken D, van Hardenbroek M, Heiri O (2016) Spatiotemporal patterns in methane flux and gas transfer velocity at low wind speeds: implications for upscaling studies on small lakes. J Geophys Res Biogeosci 121:1–12

    Article  Google Scholar 

  • Schwoerbel J (1994) Methoden der Hydrobiologie, Süßwasserbiologie. Gustav Fischer Verlag, Stuttgart (UTB 979)

  • Seddon AW, Mackay AW, Baker AG, Birks HJB, Breman E, Buck CE, Ellis EC, Froyd CA, Gill JL, Gillson L (2014) Looking forward through the past: identification of 50 priority research questions in palaeoecology. J Ecol 101(1):256–267

    Article  Google Scholar 

  • Stumm W, Morgan JJ (1996) Aquatic chemistry: chemical equilibria and rates in natural waters. Wiley, New York

    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 10:757–772

    Article  Google Scholar 

  • Taipale S, Kankaala P, Tiirola M, Jones RI (2008) Whole-lake dissolved inorganic 13C additions reveal seasonal shifts in zooplankton diet. Ecology 89:463–474

    Article  Google Scholar 

  • Turney CSM (1999) Lacustrine bulk organic δ13C in the British Isles during the last glacial—Holocene transition (14-9 ka 14C BP). Arct Antarc Alp Res 31:71–81

    Article  Google Scholar 

  • Van Hardenbroek M, Heiri O, Grey J, Bodelier PLE, Verbruggen F, Lotter AF (2010) Fossil chironomid δ13C as a proxy for past methanogenic contribution to benthic food webs in lakes? J Paleolimnol 43:235–245

    Article  Google Scholar 

  • Van Hardenbroek M, Heiri O, Parmentier FJW, Bastviken D, Ilyashuk BP, Wiklund JA, Hall RI, Lotter AF (2013) Evidence for past variations in methane availability in a Siberian thermokarst lake based on δ13C of chitinous invertebrate remains. Quat Sci Rev 66:74–84

    Article  Google Scholar 

  • Van Hardenbroek M, Lotter AF, Bastviken D, Andersen TJ, Heiri O (2014) Taxon-specific δ13C analysis of chitinous invertebrate remains in sediments from Strandsjön, Sweden. J Paleolimnol 52:95–105

    Article  Google Scholar 

  • Van Hardenbroek M, Leuenberger M, Hartikainen H, Okamura B, Heiri O (2016) Bryozoan stable carbon and hydrogen isotopes: relationships between the isotopic composition of zooids, statoblasts and lake water. Hydrobiologia 765:209–223

    Article  Google Scholar 

  • Vandekerkhove J, Declerck S, Vanhove M, Brendonck L, Jeppesen E, Porcuna Conde JM, De Meester L (2004) Use of ephippial morphology to assess richness of anomopods: potentials and pitfalls. J Limnol 63(Suppl. 1):75–84

    Article  Google Scholar 

  • Verbruggen F, Heiri O, Reichart G-J, Lotter AF (2010) Chironomid δ18O as a proxy for past lake water δ18O: a lateglacial record from Rotsee (Switzerland). Quat Sci Rev 29:2271–2279

    Article  Google Scholar 

  • Vuorio K, Meili M, Sarvala J (2006) Taxon-specific variation in the stable isotopic signatures (d13C and d15N) of lake phytoplankton. Freshw Biol 51:807–822

    Article  Google Scholar 

  • Wood TS, Okamura B (2005) A new key to the freshwater bryozoans of Britain, Ireland and Continental Europe, with notes on their ecology. Freshwater Biological Association, London

    Google Scholar 

  • Wooller MJ, Pohlman JW, Gaglioti BV, Langdon P, Jones M, Walter Anthony KM, Becker KW, Hinrichs K-U, Elvert M (2012) Reconstruction of past methane availability in an Arctic Alaska wetland indicates climate influenced methane release during the past ~12,000 years. J Paleolimnol 48:27–42

    Article  Google Scholar 

  • Zeh M, Scheidegger D, Hoehn E, Zbären D, Maurer V (2004) Kleinseen 2003. Amt für Gewässerschutz und Abfallwirtschaft des Kantons Bern, Gewässer-und Bodenschutzlabor (GBL) (eds), Bern

Download references

Acknowledgements

We thank Clemens Stampfli, Studienzentrum Gerzensee and the Stiftung der Schweizerischen Nationalbank for granting access to Gerzensee, Daniel Steiner for assistance with chlorophyll a measurements and Carole Adolf for providing the sediment trap material. This research was supported by the European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement No. 239858 (RECONMET).

Author information

Authors and Affiliations

  1. Institute of Plant Sciences and Oeschger Centre for Climate Change Research, University of Bern, Altenbergrain 21, 3013, Bern, Switzerland

    M. A. Morlock, J. Schilder, M. van Hardenbroek & O. Heiri

  2. Geography and Environment, University of Southampton, Southampton, SO17 1BJ, UK

    M. van Hardenbroek

  3. Department of Chemistry and Biochemistry and Oeschger Centre for Climate Change Research, University of Bern, Freiestrasse 3, 3012, Bern, Switzerland

    S. Szidat

  4. Alaska Stable Isotope Facility, University of Alaska Fairbanks, Fairbanks, AK, 99775, USA

    M. J. Wooller

Authors
  1. M. A. Morlock
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Schilder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. van Hardenbroek
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Szidat
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. J. Wooller
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. O. Heiri
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. A. Morlock.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Dissolved CO2 ([CO2]aq) and CH4 ([CH4]aq) concentrations for surface (0.7 m water depth) and bottom waters (8 m water depth) at the lake centre (location C1) over the fieldwork period in 2012–2014 (TIFF 16086 kb)

Fig. S2

(a) Relationship between surface water chlorophyll a concentrations (0.7 m water depth) and Daphnia δ13C at the lake centre (location C1); (b) relationship between log-transformed bottom water dissolved CH4 concentrations ([CH4]aq) (8 m water depth) and Daphnia δ13C at the lake centre (location C1); (c) relationship of the difference between particulate organic matter (POM) δ13C and Daphnia δ13C in the surface water (Δ13CPOM–Daph) and bottom water (8 m water depth) [CH4]aq; (d) surface (0.7 m water depth) and bottom water (8 m water depth) POM δ13C at the lake centre (location C1) (TIFF 31320 kb)

Table S1

Samples collected and analysed in the course of repeated fieldwork on Gerzensee between October 2012 and July 2014. “x” denotes that a sample was collected, “-” shows where no sample was collected (TIFF 8565 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morlock, M.A., Schilder, J., van Hardenbroek, M. et al. Seasonality of cladoceran and bryozoan resting stage δ13C values and implications for their use as palaeolimnological indicators of lacustrine carbon cycle dynamics. J Paleolimnol 57, 141–156 (2017). https://doi.org/10.1007/s10933-016-9936-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10933-016-9936-9

Keywords

Search

Navigation