, Volume 765, Issue 1, pp 209–223 | Cite as

Bryozoan stable carbon and hydrogen isotopes: relationships between the isotopic composition of zooids, statoblasts and lake water

  • M. van Hardenbroek
  • M. Leuenberger
  • H. Hartikainen
  • B. Okamura
  • O. Heiri
Primary Research Paper


We explored the extent to which δ13C and δD values of freshwater bryozoan statoblasts can provide information about the isotopic composition of zooids, bryozoan food and surrounding water. Bryozoan samples were collected from 23 sites and encompassed ranges of nearly 30‰ for δ13C and 100‰ for δD values. δ13C offsets between zooids and statoblasts generally ranged from −3 to +4.5‰, with larger offsets observed in four samples. However, a laboratory study with Plumatella emarginata and Lophopus crystallinus demonstrated that, in controlled settings, zooids had only 0–1.2‰ higher δ13C values than statoblasts, and 1.7‰ higher values than their food. At our field sites, we observed a strong positive correlation between median δ13C values of zooids and median δ13C values of corresponding statoblasts. We also observed a positive correlation between median δD values of zooids and statoblasts for Plumatella, and a positive correlation between median δD values of statoblasts and δD values of lake water for Plumatella and when all bryozoan taxa were examined together. Our results suggest that isotope measurements on statoblasts collected from flotsam or sediment samples can provide information on the feeding ecology of bryozoans and the H isotopic composition of lake water.


Freshwater Bryozoa Stable isotopes Statoblasts Lakes Feeding ecology Palaeoecology 



We thank Michiel van der Waaij for collecting samples in Dutch lakes and for useful information on the habitat and ecology of several freshwater bryozoan species ( Winfried Lampert, Peter Hammond, Alex Gruhl, and Elena Brand greatly helped during an exploratory field trip. Robert Dünner is kindly acknowledged for suggesting locations in a number of Swiss lakes. Peter Nyfeler’s work analysing the stable isotope data has been invaluable. We thank four anonymous reviewers for their comments on earlier versions of this manuscript. This study was funded by the European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement no. 239858 (RECONMET).


  1. Agasild, H., P. Zingel, L. Tuvikene, A. Tuvikene, H. Timm, T. Feldmann, J. Salujõe, K. Toming, R. I. Jones & T. Nõges, 2014. Biogenic methane contributes to the food web of a large, shallow lake. Freshwater Biology 59: 272–285.CrossRefGoogle Scholar
  2. Belle, S., C. Parent, V. Frossard, V. R. Verneaux, L. Millet, P.-M. Chronopoulou, P. Sabatier & M. Magny, 2014. Temporal changes in the contribution of methane-oxidizing bacteria to the biomass of chironomid larvae determined using stable carbon isotopes and ancient DNA. Journal of Paleolimnology 52: 215–228.CrossRefGoogle Scholar
  3. Bowen, G. J., 2014. The Online Isotopes in Precipitation Calculator, version 2.2.
  4. Bowen, G. J. & J. Revenaugh, 2003. Interpolating the isotopic composition of modern meteoric precipitation. Water Resources Research 39: 1299.CrossRefGoogle Scholar
  5. Deines, P., M. J. Wooller & J. Grey, 2009. Unraveling complexities in benthic food webs using a dual stable isotope (hydrogen and carbon) approach. Freshwater Biology 54: 2243–2251.CrossRefGoogle Scholar
  6. DeNiro, M. J. & S. Epstein, 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica and Cosmochimica Acta 42: 495–506.CrossRefGoogle Scholar
  7. Filot, M. S., M. Leuenberger, A. Pazdur & T. Boettger, 2006. Rapid online equilibration method to determine the D/H ratios of non-exchangeable hydrogen in cellulose. Rapid Communications in Mass Spectrometry 20: 3337–3344.CrossRefPubMedGoogle Scholar
  8. France, R. L., 1995. Differentiation between littoral and pelagic food webs in lakes using stable carbon isotopes. Limnology and Oceanography 40: 1310–1313.CrossRefGoogle Scholar
  9. Francis, D., 2001. Bryozoan Statoblasts. In Smol, J., H. J. Birks & W. Last (eds), Tracking Environmental Change Using Lake Sediments. Developments in Paleoenvironmental Research, Vol. 4. Springer, Dordrecht: 105–123.CrossRefGoogle Scholar
  10. Frey, D. G., 1964. Remains of animals in Quaternary lake and bog sediments and their interpretation. Archiv für Hydrobiologie Supplement 2: 1–114.Google Scholar
  11. Frossard, V., S. Belle, V. Verneaux, L. Millet & M. Magny, 2013. A study of the δ13C offset between chironomid larvae and their exuvial head capsules: implications for palaeoecology. Journal of Paleolimnology 50: 379–386.CrossRefGoogle Scholar
  12. Frossard, V., V. Verneaux, L. Millet, J.-P. Jenny, F. Arnaud, M. Magny & M.-E. Perga, 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. Freshwater Biology 59: 789–802.CrossRefGoogle Scholar
  13. Gat, J. R., 1995. Stable Isotopes of Fresh and Saline Lakes. In Lerman, A., D. M. Imboden & J. R. Gat (eds), Physics and Chemistry of Lakes. Springer, Berlin: 139–195.CrossRefGoogle Scholar
  14. Grey, J., S. Waldron & R. Hutchinson, 2004a. The utility of carbon and nitrogen isotope analyses to trace contributions from fish farms to the receiving communities of freshwater lakes: a pilot study in Esthwaite Water, UK. Hydrobiologia 524: 253–262.CrossRefGoogle Scholar
  15. Grey, J., A. Kelly, S. Ward, N. Sommerwerk & R. I. Jones, 2004b. Seasonal changes in the stable isotope values of lake-dwelling chironomid larvae in relation to feeding and life cycle variability. Freshwater Biology 49: 681–689.CrossRefGoogle Scholar
  16. Hammer, Ø., D. A. T. Harper, & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 9 pp.Google Scholar
  17. Hartikainen, H. & B. Okamura, 2012. Castrating parasites and colonial hosts. Parasitology 139: 547–556.CrossRefPubMedGoogle Scholar
  18. Heiri, O., J. Schilder & M. van Hardenbroek, 2012. Stable isotopic analysis of fossil chironomids as an approach to environmental reconstruction: state of development and future challenges. Fauna Norvegica 31: 7–18.CrossRefGoogle Scholar
  19. Hill, S. L. L., C. D. Sayer, P. M. Hammond, V. K. Rimmer, T. A. Davidson, D. J. Hoare, A. Burgess & B. Okamura, 2007. Are rare species rare or just overlooked? Assessing the distribution of the freshwater bryozoan, Lophopus crystallinus. Biological Conservation 135: 223–234.CrossRefGoogle Scholar
  20. Hobson, K. A., L. Atwell & L. I. Wassenaar, 1999. Influence of drinking water and diet on the stable-hydrogen isotope ratios of animal tissues. Proceedings of the National Academy of Sciences of the United States of America 96: 8003–8006.PubMedCentralCrossRefPubMedGoogle Scholar
  21. Jones, R. I. & J. Grey, 2011. Biogenic methane in freshwater food webs. Freshwater Biology 56: 213–229.CrossRefGoogle Scholar
  22. Jones, R. I., J. Grey, D. Sleep & L. Arvola, 1999. Stable isotope analysis of zooplankton carbon nutrition in humic lakes. Oikos 86: 97–104.CrossRefGoogle Scholar
  23. Kaminski, M., 1984. Food composition of three bryozoan species (Bryozoa, Phylactolaemata) in a mesotrophic lake. Polish Archive of Hydrobiology 31: 45–53.Google Scholar
  24. Kankaala, P., S. Taipale, L. Li & R. Jones, 2010. Diets of crustacean zooplankton, inferred from stable carbon and nitrogen isotope analyses, in lakes with varying allochthonous dissolved organic carbon content. Aquatic Ecology 44: 781–795.CrossRefGoogle Scholar
  25. Karlsson, J., M. Berggren, J. Ask, P. Byström, A. Jonsson, H. Laudon & M. Jansson, 2012. Terrestrial organic matter support of lake food webs: evidence from lake metabolism and stable hydrogen isotopes of consumers. Limnology and Oceanography 57: 1042–1048.CrossRefGoogle Scholar
  26. Lacourt, A., 1968. A monograph of the freshwater Bryozoa-Phylactolaemata. Zoologische Verhandelungen 93: 1–155.Google Scholar
  27. McCutchan, J. H., W. M. Lewis, C. Kendall & C. C. McGrath, 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378–390.CrossRefGoogle Scholar
  28. Okamura, B., K. Ayres, J. Salgado, T. Davidson, R. Shaw, T. Stephens, D. Hoare & C. Sayer, 2013. Shallow lake sediments provide evidence for metapopulation dynamics: a pilot study. Aquatic Ecology 47: 163–176.CrossRefGoogle Scholar
  29. Perga, M.-E., 2011. Taphonomic and early diagenetic effects on the C and N stable isotope composition of cladoceran remains: implications for paleoecological studies. Journal of Paleolimnology 46: 203–213.CrossRefGoogle Scholar
  30. Peters, L., C. Faust & W. Traunspurger, 2012. Changes in community composition, carbon and nitrogen stable isotope signatures and feeding strategy in epilithic aquatic nematodes along a depth gradient. Aquatic Ecology 46: 371–384.CrossRefGoogle Scholar
  31. Post, D. M., 2002. Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83: 703–718.CrossRefGoogle Scholar
  32. Power, M., K. R. R. A. Guiguer & D. R. Barton, 2003. Effects of temperature on isotopic enrichment in Daphnia magna: implications for aquatic food-web studies. Rapid Communications in Mass Spectrometry 17: 1619–1625.CrossRefPubMedGoogle Scholar
  33. R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  34. Richelle, E., Z. Moureau & G. Van de Vyver, 1994. Bacterial feeding by the freshwater bryozoan Plumatella fungosa (Pallas, 1768). Hydrobiologia 291: 193–199.CrossRefGoogle Scholar
  35. Schilder, J., C. Tellenbach, M. Möst, P. Spaak, M. van Hardenbroek, M. J. Wooller & O. Heiri, 2015a. Experimental assessment of environmental influences on the stable isotopic composition of Daphnia pulicaria and their ephippia. Biogeosciences 12: 3819–3830.CrossRefGoogle Scholar
  36. Schilder, J., D. Bastviken, M. van Hardenbroek, M. Leuenberger, P. Rinta, T. Stötter & O. Heiri, 2015b. The stable carbon isotopic composition of Daphnia ephippia in small, temperate lakes reflects in-lake methane availability. Limnology and Oceanography 60: 1064–1075.CrossRefGoogle Scholar
  37. Schimmelmann, A., A. L. Sessions & M. Mastalerz, 2006. Hydrogen isotopic (D/H) composition of organic matter during diagenesis and thermal maturation. Annual Review of Earth and Planetary Sciences 34: 501–533.CrossRefGoogle Scholar
  38. Schürch, M., R. Kozel, U. Schotterer & J.-P. Tripet, 2003. Observation of isotopes in the water cycle – the Swiss National Network (NISOT). Environmental Geology 45: 1–11.CrossRefGoogle Scholar
  39. Solomon, C., J. Cole, R. Doucett, M. Pace, N. Preston, L. Smith & B. Weidel, 2009. The influence of environmental water on the hydrogen stable isotope ratio in aquatic consumers. Oecologia 161: 313–324.CrossRefPubMedGoogle Scholar
  40. Soto, D. X., L. I. Wassenaar & K. A. Hobson, 2013. Stable hydrogen and oxygen isotopes in aquatic food webs are tracers of diet and provenance. Functional Ecology 27: 535–543.CrossRefGoogle Scholar
  41. Taipale, S., P. Kankaala & R. I. Jones, 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.CrossRefGoogle Scholar
  42. Turney, C. S. M., 1999. Lacustrine bulk organic δ13C in the British Isles during the last glacial-Holocene transition (14-9 ka C-14 BP). Arctic Antarctic and Alpine Research 31: 71–81.CrossRefGoogle Scholar
  43. Vander Zanden, M. J. & J. B. Rasmussen, 1999. Primary consumer δ13C and δ15N and the trophic position of aquatic consumers. Ecology 80: 1395–1404.CrossRefGoogle Scholar
  44. Van Hardenbroek, M., O. Heiri, J. Grey, P. Bodelier, F. Verbruggen & A. F. Lotter, 2010. Fossil chironomid δ13C as a proxy for past methanogenic contribution to benthic food webs in lakes? Journal of Paleolimnology 43: 235–245.CrossRefGoogle Scholar
  45. Van Hardenbroek, M., O. Heiri, F. J. W. Parmentier, D. Bastviken, B. P. Ilyashuk, J. A. Wiklund, R. I. Hall & A. F. Lotter, 2013a. Evidence for past variations in methane availability in a Siberian thermokarst lake based on δ13C of chitinous invertebrate remains. Quaternary Science Reviews 66: 74–84.CrossRefGoogle Scholar
  46. Van Hardenbroek, M., D. R. Gröcke, P. E. Sauer & S. A. Elias, 2013b. North American transect of stable hydrogen and oxygen isotopes in water beetles from a museum collection. Journal of Paleolimnology 48: 461–470.CrossRefGoogle Scholar
  47. Van Hardenbroek, M., A. F. Lotter, D. Bastviken, T. J. Andersen & O. Heiri, 2014. Taxon-specific δ13C analysis of chitinous invertebrate remains in sediments from Strandsjön, Sweden. Journal of Paleolimnology 52: 95–105.CrossRefGoogle Scholar
  48. Van Riel, M. C., G. Velde, S. Rajagopal, S. Marguillier, F. Dehairs & A. B. Vaate, 2006. Trophic Relationships in the Rhine Food Web During Invasion and After Establishment of the Ponto-Caspian Invader Dikerogammarus Villosus. In Leuven, R. S. E. W., A. M. J. Ragas, A. J. M. Smits & G. Velde (eds), Living Rivers: Trends and Challenges in Science and Management, Developments in Hydrobiology. Springer, Dordrecht: 39–58.CrossRefGoogle Scholar
  49. Vuorio, K., M. Meili & J. Sarvala, 2006. Taxon-specific variation in the stable isotopic signatures (δ13C and δ15N) of lake phytoplankton. Freshwater Biology 51: 807–822.CrossRefGoogle Scholar
  50. Wang, Y., D. O’Brien, J. Jenson, D. Francis & M. Wooller, 2009. The influence of diet and water on the stable oxygen and hydrogen isotope composition of Chironomidae (Diptera) with paleoecological implications. Oecologia 160: 225–233.CrossRefPubMedGoogle Scholar
  51. Wassenaar, L. I. & K. A. Hobson, 2000. Improved method for determining the stable-hydrogen isotopic composition (δD) of complex organic materials of environmental interest. Environtal Science & Technology 34: 2354–2360.CrossRefGoogle Scholar
  52. Whiticar, M. J., 1999. Carbon and hydrogen isotope systematics of bacterial formation and oxidation of methane. Chemical Geology 161: 291–314.CrossRefGoogle Scholar
  53. Wood, T. S. & B. Okamura, 2005. A New Key to Freshwater Bryozoans of Britain, Ireland and Continental Europe, With Notes on Their Ecology. Freshwater Biological Association, London.Google Scholar
  54. Wooller, M. J., D. Francis, M. L. Fogel, G. H. Miller, I. R. Walker & A. P. Wolfe, 2004. Quantitative paleotemperature estimates from δ18O of chironomid head capsules preserved in arctic lake sediments. Journal of Paleolimnology 31: 267–274.CrossRefGoogle Scholar
  55. Wooller, M. J., Y. Wang & Y. Axford, 2008. A multiple stable isotope record of Late Quaternary limnological changes and chironomid paleoecology from northeastern Iceland. Journal of Paleolimnology 40: 63–77.CrossRefGoogle Scholar
  56. Wooller, M., J. Pohlman, B. Gaglioti, P. Langdon, M. Jones, K. Walter Anthony, K. Becker, K.-U. Hinrichs & M. Elvert, 2012. Reconstruction of past methane availability in an Arctic Alaska wetland indicates climate influenced methane release during the past ~ 12,000 years. Journal of Paleolimnology 48: 27–42.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  1. 1.Institute of Plant Sciences and Oeschger Centre for Climate Change ResearchUniversity of BernBernSwitzerland
  2. 2.Geography and EnvironmentUniversity of SouthamptonSouthamptonUK
  3. 3.Physics Institute and Oeschger Centre for Climate Change ResearchUniversity of BernBernSwitzerland
  4. 4.Department of Life SciencesNatural History MuseumLondonUK
  5. 5.EAWAG, Department of Aquatic Ecology and ETH-ZurichInstitute of Integrative Biology (IBZ)DübendorfSwitzerland

Personalised recommendations