Journal of Paleolimnology

, Volume 52, Issue 1–2, pp 95–105 | Cite as

Taxon-specific δ13C analysis of chitinous invertebrate remains in sediments from Strandsjön, Sweden

  • M. van Hardenbroek
  • A. F. Lotter
  • D. Bastviken
  • T. J. Andersen
  • O. Heiri
Original paper


Taxon-specific stable carbon isotope (δ13C) analysis of chitinous remains of invertebrates can provide valuable information about the carbon sources used by invertebrates living in specific habitats of lake ecosystems (for example, sediments, water column, or aquatic vegetation). This is complementary to δ13C of sedimentary organic matter (SOM), which provides an integrated signal of organic matter produced in a lake and its catchment, and of diagenetic processes within sediments. In a sediment record from Strandsjön (Sweden) covering the past circa 140 years, we analyzed SOM geochemistry (δ13C, C:Natomic, organic carbon content) and δ13C of chitinous invertebrate remains in order to examine whether taxon-specific δ13C records could be developed for different invertebrate groups and whether these analyses provide insights into past changes of organic carbon sources for lacustrine invertebrates available in benthic and planktonic compartments of the lake. Invertebrate taxa included benthic chironomids (Chironomus, Chironomini excluding Chironomus, Tanytarsini, and Tanypodinae), filter-feeders on suspended particulate organic matter (Daphnia, Plumatella and Cristatella mucedo), and Rhabdocoela. δ13C of chironomid remains indicated periodic availability of 13C-depleted carbon sources in the benthic environment of the lake as δ13C values of the different chironomid taxa fluctuated simultaneously between −34.7 and −30.5 ‰ (VPDB). Daphnia and Bryozoa showed parallel changes in their δ13C values which did not coincide with variations in δ13C of chironomids, though, and a 2–3 ‰ decrease since circa AD 1960. The decrease in δ13C of Daphnia and Bryozoa could indicate a decrease in phytoplankton δ13C as a result of lower lake productivity, which is in accordance with historical information about the lake that suggests a shift to less eutrophic conditions after AD 1960. In contrast, Rhabdocoela cocoons were characterized by relatively high δ13C values (−30.4 to −28.2 ‰) that did not show a strong temporal trend, which could be related to the predatory feeding mode and wide prey spectrum of this organism group. The taxon-specific δ13C analyses of invertebrate remains indicated that different carbon sources were available for the benthic chironomid larvae than for the filter-feeding Daphnia and bryozoans. Our results therefore demonstrate that taxon-specific analysis of δ13C of organic invertebrate remains can provide complementary information to measurements on bulk SOM and that δ13C of invertebrate remains may allow the reconstruction of past changes in carbon sources and their δ13C in different habitats of lake ecosystems.


Invertebrates Chitinous remains Lake sediment Stable carbon isotopes Sedimentary organic matter 



We thank Lotta Frisk Hagström and Kristina Eriksson for valuable historical information about the lake and Arndt Schimmelmann and three anonymous reviewers for their helpful suggestions to improve this manuscript. This research was supported by the Darwin Centre for Biogeosciences, the European Research Council (ERC) Starting Grant project RECONMET (Project No. 239858), and the Swedish Research Council (Project No. VR 2006-3256).

Supplementary material

10933_2014_9780_MOESM1_ESM.xls (26 kb)
Supplementary material 1 (XLS 25 kb)


  1. Appleby PG (2001) Chronostratigraphic techniques in recent sediments. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments. Volume 1: Basin analysis, coring, and chronological techniques. Kluwer Academic Publishers, Dordrecht, pp 171–203Google Scholar
  2. Appleby PG, Oldfield F (1978) The calculation of lead-210 dates assuming a constant rate of supply of unsupported 210Pb to the sediment. Catena 5:1–8CrossRefGoogle Scholar
  3. Bade D, Pace M, Cole J, Carpenter S (2006) Can algal photosynthetic inorganic carbon isotope fractionation be predicted in lakes using existing models? Aquat Sci 68:142–153CrossRefGoogle Scholar
  4. Barker PA, Hurrell ER, Leng MJ, Verschuren D, Conley D, Plessens B (2013) The changing carbon cycle of lakes revealed by the stable isotopes of diatom silica: a 25 ka record from Lake Challa, Kilimanjaro. Quat Sci Rev 66:55–63CrossRefGoogle Scholar
  5. Brenner M, Whitmore TJ, Curtis JH, Hodell DA, Schelske CL (1999) Stable isotope (δ13C and δ15N) signatures of sedimented organic matter as indicators of historic lake trophic state. J Paleolimnol 22:205–221CrossRefGoogle Scholar
  6. Brooks SJ, Langdon PG, Heiri O (2007) The identification and use of Palaearctic Chironomidae larvae in palaeoecolgy. QRA technical guide no. 10. Quaternary Research Association, LondonGoogle Scholar
  7. Brunberg A-K, Blomqvist P (1998) Vatten i Uppsala län 1997. Beskrivning, utvärdering, åtgärdsförslag. Rapport nr 8/1998. Upplandsstiftelsen. (in Swedish)Google Scholar
  8. DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506CrossRefGoogle Scholar
  9. France RL (1995a) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312CrossRefGoogle Scholar
  10. France RL (1995b) Stable isotopic survey of the role of macrophytes in the carbon flow of aquatic foodwebs. Vegetatio 124:67–72CrossRefGoogle Scholar
  11. Frey DG (1964) Remains of animals in Quaternary lake and bog sediments and their interpretation. Adv Limnol 2:1–114Google Scholar
  12. Frossard V, Belle S, Verneaux V, Millet L, Magny M (2013) A study of the δ13C offset between chironomid larvae and their exuvial head capsules: implications for palaeoecology. J Paleolimnol 50:379–386CrossRefGoogle Scholar
  13. 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. doi: 10.1111/fwb.12304 Google Scholar
  14. Geller W, Müller H (1981) The filtration apparatus of Cladocera: filter mesh-sizes and their implications on food selectivity. Oecologia 49:316–321CrossRefGoogle Scholar
  15. 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. In: Proceedings of the 18th international symposium on chironomidae, Trondheim 4–6. August 2011, Fauna Norvegica 31:7–18Google Scholar
  16. Herzschuh U, Mischke S, Meyer H, Plessen B, Zhang C (2010) Lake nutrient variability inferred from elemental (C, N, S) and isotopic (δ13C, δ15N) analyses of aquatic plant macrofossils. Quat Sci Rev 29:2161–2172CrossRefGoogle Scholar
  17. Hollander DJ, McKenzie JA, Hsu KJ, Huc AY (1993) Application of an eutrophic lake model to the origin of ancient organic-carbon-rich sediments. Glob Biogeochem Cycles 7:157–179CrossRefGoogle Scholar
  18. Hurrell ER, Barker PA, Leng MJ, Vane CH, Wynn P, Kendrick CP, Verschuren D, Street-Perrott FA (2011) Developing a methodology for carbon isotope analysis of lacustrine diatoms. Rapid Commun Mass Spectrom 25:1567–1574CrossRefGoogle Scholar
  19. Jennings JB (1957) Studies on feeding, digestion, and food storage in free-living flatworms (Platyhelminthes: Turbellaria). Biol Bull 112:63–80CrossRefGoogle Scholar
  20. Jones RI, Carter CE, Kelly A, Ward S, Kelly DJ, Grey J (2008) Widespread contribution of methane-cycle bacteria to the diets of lake profundal chironomid larvae. Ecology 89:857–864CrossRefGoogle Scholar
  21. Kaminski M (1984) Food composition of three bryozoan species (Bryozoa, Phylactolaemata) in a mesotrophic lake. P Arch Hydrobiol 31:45–53Google Scholar
  22. Kiyashko SI, Narita T, Wada E (2001) Contribution of methanotrophs to freshwater macroinvertebrates: evidence from stable isotope ratios. Aquat Microb Ecol 24:203–207CrossRefGoogle Scholar
  23. Kolasa J, Tyler S (2010) Flatworms: Turbellaria and Nemertea. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, London, pp 143–161CrossRefGoogle Scholar
  24. Leavitt PR, Brock CS, Ebel C, Patoine A (2006) Landscape-scale effects of urban nitrogen on a chain of freshwater lakes in central North America. Limnol Oceanogr 51:2262–2277CrossRefGoogle Scholar
  25. Leng MJ, Lamb AL, Marshall JD, Wolfe BB, Jones MD, Holmes JA, Arrowsmith C (2005) Isotopes in lake sediments. In: Leng MJ (ed) Isotopes in palaeoenvironmental research. Springer, Dordrecht, pp 147–184Google Scholar
  26. Luther A (1955) Die Dalyelliiden (Turbellaria Neorhabdocoela), eine monografie. von Tilgmann, HelsingforsGoogle Scholar
  27. Macko SA, Helleur R, Hartley G, Jackman P (1990) Diagenesis of organic matter—a study using stable isotopes of individual carbohydrates. Org Geochem 16:1129–1137CrossRefGoogle Scholar
  28. Merritt RW, Cummins KW, Berg MB (2008) An introduction to the aquatic insects of North America. Kendall and Hunt, DubuqueGoogle Scholar
  29. Meyers PA, Lallier-Vergès E (1999) Lacustrine sedimentary organic matter records of late Quaternary paleoclimates. J Paleolimnol 21:345–372CrossRefGoogle Scholar
  30. Meyers PA, Teranes JL (2001) Sediment organic matter. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments. Volume 2: Physical and Geochemical Techniques. Kluwer Academic Publishers, Dordrecht, pp 239–269Google Scholar
  31. Mihuc T, Toetz D (1994) Determination of diets of alpine aquatic insects using stable isotopes and gut analysis. Am Midl Nat 131:146–155CrossRefGoogle Scholar
  32. Moller Pillot HKM (2009) Chironomidae larvae, biology and ecology of the Chironomini. KNNV Publishing, ZeistGoogle Scholar
  33. Moog O (2002) Fauna Aquatica Austriaca. Wasserwirtshcaftskataster, Bundesministerium für Land- und Forstwirtschaft, Umwelt und Wasserwirtschaft, ViennaGoogle Scholar
  34. Okamura B, Hatton-Ellis T (1995) Population biology of bryozoans: correlates of sessile, colonial life histories in freshwater habitats. Cell Mol Life Sci 51:510–525CrossRefGoogle Scholar
  35. Perga M-E (2010) Potential of δ13C and δ15N of cladoceran subfossil exoskeletons for paleo-ecological studies. J Paleolimnol 44:387–395CrossRefGoogle Scholar
  36. 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 46:203–213CrossRefGoogle Scholar
  37. Rau GH (1980) Carbon-13/carbon-12 variation in subalpine lake aquatic insects: food source implications. Can J Fish Aquat Sci 37:742–746CrossRefGoogle Scholar
  38. Schimmelmann A (2011) Carbon, nitrogen and oxygen stable isotope ratios in chitin. In: Gupta NS (ed) Chitin. Springer, Netherlands, pp 81–103CrossRefGoogle Scholar
  39. Stevenson FJ (1982) Extraction, fractionation, and general chemical composition of soil organic matter. In: Stevenson FJ (ed) Humus chemistry. Genesis, composition, reactions. Wiley, New York, pp 26–54Google Scholar
  40. Turney CSM (1999) Lacustrine bulk organic δ13C in the British Isles during the last Glacial-Holocene transition (14-9 ka 14C BP). Arct Antarct Alp Res 31:71–81Google Scholar
  41. Vallenduuk H, Moller Pillot HKM (2007) Chironomidae larvae, general introduction and Tanypodinae. KNNV Publishing, ZeistGoogle Scholar
  42. van Hardenbroek M, Heiri O, Grey J, Bodelier P, Verbruggen F, Lotter A (2010a) Fossil chironomid δ13C as a proxy for past methanogenic contribution to benthic food webs in lakes? J Paleolimnol 43:235–245CrossRefGoogle Scholar
  43. van Hardenbroek M, Heiri O, Lotter A (2010b) Efficiency of different mesh sizes for isolating fossil chironomids for stable isotope and radiocarbon analyses. J Paleolimnol 44:721–729CrossRefGoogle Scholar
  44. van Hardenbroek M, Lotter AF, Bastviken D, Duc NT, Heiri O (2012) Relationship between δ13C of chironomid remains and methane flux in Swedish lakes. Freshw Biol 57:166–177CrossRefGoogle Scholar
  45. 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 66:74–84CrossRefGoogle Scholar
  46. Vander Zanden MJ, Rasmussen JB (1999) Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80:1395–1404CrossRefGoogle Scholar
  47. Vanderkerkhove J, Declerck S, Vanhove M, Brendonck L, Jeppesen E, Porcuna JM, De Meester L (2004) Use of ephippial morphology to assess richness of anomopods: potentials and pitfalls. J Limnol 63:75–84Google Scholar
  48. Verbruggen F, Heiri O, Reichart GJ, De Leeuw J, Nierop K, Lotter A (2010) Effects of chemical pretreatments on δ18O measurements, chemical composition, and morphology of chironomid head capsules. J Paleolimnol 43:857–872CrossRefGoogle Scholar
  49. Wood TS, Okamura B (2005) A new key to freshwater bryozoans of Britain, Ireland and continental Europe, with notes on their ecology. Freshwater Biological Association, LondonGoogle Scholar
  50. Wooller MJ, Wang Y, Axford Y (2008) A multiple stable isotope record of late Quaternary limnological changes and chironomid paleoecology from northeastern Iceland. J Paleolimnol 40:63–77CrossRefGoogle Scholar
  51. Wooller M, Pohlman J, Gaglioti B, Langdon P, Jones M, Walter Anthony K, Becker K, 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 48:27–42CrossRefGoogle Scholar
  52. Zemskaya T, Sitnikova T, Kiyashko S, Kalmychkov G, Pogodaeva T, Mekhanikova I, Naumova T, Shubenkova O, Chernitsina S, Kotsar O, Chernyaev E, Khlystov O (2012) Faunal communities at sites of gas- and oil-bearing fluids in Lake Baikal. Geo-Mar Lett 32:437–451CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • M. van Hardenbroek
    • 1
    • 2
  • A. F. Lotter
    • 2
  • D. Bastviken
    • 3
  • T. J. Andersen
    • 4
  • O. Heiri
    • 1
  1. 1.Institute of Plant Sciences and Oeschger Centre for Climate Change ResearchUniversity of BernBernSwitzerland
  2. 2.Palaeoecology, Laboratory of Palaeobotany and Palynology, Department of Physical GeographyUtrecht UniversityUtrechtThe Netherlands
  3. 3.Department of Thematic Studies - Water and Environmental StudiesLinköping UniversityLinköpingSweden
  4. 4.Department of Geography and GeologyUniversity of CopenhagenCopenhagen KDenmark

Personalised recommendations