Advertisement

Ambio

, Volume 47, Issue 8, pp 884–892 | Cite as

Effects of an invasive polychaete on benthic phosphorus cycling at sea basin scale: An ecosystem disservice

  • Antonia Nyström Sandman
  • Johan Näslund
  • Ing-Marie Gren
  • Karl Norling
Research Article
  • 89 Downloads

Abstract

Macrofaunal activities in sediments modify nutrient fluxes in different ways including the expression of species-specific functional traits and density-dependent population processes. The invasive polychaete genus Marenzelleria was first observed in the Baltic Sea in the 1980s. It has caused changes in benthic processes and affected the functioning of ecosystem services such as nutrient regulation. The large-scale effects of these changes are not known. We estimated the current Marenzelleria spp. wet weight biomass in the Baltic Sea to be 60–87 kton (95% confidence interval). We assessed the potential impact of Marenzelleria spp. on phosphorus cycling using a spatially explicit model, comparing estimates of expected sediment to water phosphorus fluxes from a biophysical model to ecologically relevant experimental measurements of benthic phosphorus flux. The estimated yearly net increases (95% CI) in phosphorous flux due to Marenzelleria spp. were 4.2–6.1 kton based on the biophysical model and 6.3–9.1 kton based on experimental data. The current biomass densities of Marenzelleria spp. in the Baltic Sea enhance the phosphorus fluxes from sediment to water on a sea basin scale. Although high densities of Marenzelleria spp. can increase phosphorus retention locally, such biomass densities are uncommon. Thus, the major effect of Marenzelleria seems to be a large-scale net decrease in the self-cleaning capacity of the Baltic Sea that counteracts human efforts to mitigate eutrophication in the region.

Keywords

Benthic–pelagic coupling Ecosystem services Eutrophication Invasive species Nutrient cycling 

Notes

Acknowledgements

The authors would like to thank the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS) and Swedish Environmental Protection Agency (Naturvårdsverket) for financial support (VALUES Project), and Stockholm Marina Forskningscentrum (Östersjöcentrum) for time and space at Askö Laboratory; Andrey Sikorski for taxonomic expertise; Mats Westerbom for help with the OIVA database; Joanna Norkko, Ragnar Elmgren, Anna-Stiina Heiskanen, Eva Roth, and Gunilla Ejdung for valuable comments on the study; Two anonymous reviewers and the editor, whose comments greatly improved the manuscript; HELCOM as well as laboratory and field staff contributing to the benthic monitoring of the Baltic Sea.

Supplementary material

13280_2018_1050_MOESM1_ESM.pdf (982 kb)
Supplementary material 1 (PDF 983 kb)
13280_2018_1050_MOESM2_ESM.tif (3 mb)
Supplementary material 2 (TIFF 3076 kb)
13280_2018_1050_MOESM3_ESM.tif (2.7 mb)
Supplementary material 3 (TIFF 2768 kb)

References

  1. Al-Hamdani, Z., and J. Reker, ed. Towards marine landscapes in the Baltic Sea, Vol. #10. BALANCE Interim Report, 2007. http://balance-eu.org/. Accessed 04 March 2015.
  2. Bick, A. 2005. A new Spionidae (Polychaeta) from North Carolina and a redescription of Marenzelleria wireni Augener, 1913, from Spitsbergen, with a key for all species of Marenzelleria. Helgoland Marine Research 59: 265–272.CrossRefGoogle Scholar
  3. Bick, A., and R. Burckhardt. 1989. First record of Marenzelleria viridis (Polychaeta, Spionidae) in the Baltic Sea, with a key to the Spionidae of the Baltic Sea. Mitteilungen aus dem Zoologischen Museum in Berlin 65: 237–247.CrossRefGoogle Scholar
  4. Blank, M., A.O. Laine, K. Juerss, and R. Bastrop. 2008. Molecular identification key based on PCR/RFLP for three polychaete sibling species of the genus Marenzelleria, and the species’ current distribution in the Baltic Sea. Helgoland Marine Research 62: 129–141.  https://doi.org/10.1007/s10152-007-0081-8.CrossRefGoogle Scholar
  5. Bonaglia, S., M. Bartoli, J.S. Gunnarsson, L. Rahm, C. Raymond, O. Svensson, S.S. Yekta, and V. Brüchert. 2013. Effect of reoxygenation and Marenzelleria spp. bioturbation on Baltic Sea sediment metabolism. Marine Ecology Progress Series 482: 43–55.CrossRefGoogle Scholar
  6. Borg, H., and P. Jonsson. 1996. Large-scale metal distribution in Baltic Sea sediments. Marine Pollution Bulletin 32: 8–21.CrossRefGoogle Scholar
  7. Breiman, L. 2001. Random forests. Machine Learning 45: 5–32.CrossRefGoogle Scholar
  8. Bučas, M., U. Bergström, A.L. Downie, G. Sundblad, M. Gullström, M. Von Numers, A. Šiaulys, and M. Lindegarth. 2013. Empirical modelling of benthic species distribution, abundance, and diversity in the Baltic Sea: Evaluating the scope for predictive mapping using different modelling approaches. ICES Journal of Marine Science.  https://doi.org/10.1093/icesjms/fst036.CrossRefGoogle Scholar
  9. Carstensen, J., D.J. Conley, E. Bonsdorff, B.G. Gustafsson, S. Hietanen, U. Janas, T. Jilbert, A. Maximov, et al. 2014. Hypoxia in the Baltic Sea: Biogeochemical cycles, benthic fauna, and management. Ambio 43: 26–36.  https://doi.org/10.1007/s13280-013-0474-7.CrossRefGoogle Scholar
  10. Chaffin, J.D., and D.D. Kane. 2010. Burrowing mayfly (Ephemeroptera: Ephemeridae: Hexagenia spp.) bioturbation and bioirrigation: A source of internal phosphorus loading in Lake Erie. Journal of Great Lakes Research 36: 57–63.CrossRefGoogle Scholar
  11. Conley, D.J., A. Stockenberg, R. Carman, R.W. Johnstone, L. Rahm, and F. Wulff. 1997. Sediment–water nutrient fluxes in the Gulf of Finland, Baltic Sea. Estuarine, Coastal and Shelf Science 45: 591–598.CrossRefGoogle Scholar
  12. Conley, D.J., C. Humborg, L. Rahm, O.P. Savchuk, and F. Wulff. 2002. Hypoxia in the Baltic Sea and basin-scale changes in phosphorus biogeochemistry. Environmental Science and Technology 36: 5315–5320.CrossRefGoogle Scholar
  13. Cutler, D.R., T.C. Edwards Jr., K.H. Beard, A. Cutler, K.T. Hess, J. Gibson, and J.J. Lawler. 2007. Random forests for classification in ecology. Ecology 88: 2783–2792.CrossRefGoogle Scholar
  14. de Groot, R.S., R. Alkemade, L. Braat, L. Hein, and L. Willemen. 2010. Challenges in integrating the concept of ecosystem services and values in landscape planning, management and decision making. Ecological Complexity 7: 260–272.CrossRefGoogle Scholar
  15. Gallepp, G.W. 1979. Chironomid influence on phosphorus release in sediment–water microcosms. Ecology 60: 547–556.CrossRefGoogle Scholar
  16. Gogina, M., H. Nygård, M. Blomqvist, D. Daunys, A.B. Josefson, J. Kotta, A. Maximov, J. Warzocha, V. Yermakov, U. Gräwe, and M.L. Zettler. 2016. The Baltic Sea scale inventory of benthic faunal communities. ICES Journal of Marine Science 73: 1196–1213.CrossRefGoogle Scholar
  17. Götting, M., S. Mikkat, M. Verleih, and R. Bastrop. 2011. Proteomic comparison of two invasive polychaete species and their naturally occurring F-1-hybrids. Journal of Proteome Research 11: 897–905.  https://doi.org/10.1021/pr200710z.CrossRefGoogle Scholar
  18. Granberg, M.E., J.S. Gunnarsson, J.E. Hedman, R. Rosenberg, and P. Jonsson. 2008. Bioturbation-driven release of organic contaminants from Baltic Sea sediments mediated by the invading polychaete Marenzelleria neglecta. Environmental Science and Technology 42: 1058–1065.CrossRefGoogle Scholar
  19. Gren, I.-M., O.P. Savchuck, and T. Jansson. 2013. Cost-effective spatial and dynamic management of a eutrophied Baltic Sea. Marine Resource Economics 28: 263–284.CrossRefGoogle Scholar
  20. Gustafsson, B.G., F. Schenk, T. Blenckner, K. Eilola, H.M. Meier, B. Müller-Karulis, T. Neumann, T. Ruoho-Airola, et al. 2012. Reconstructing the development of Baltic Sea eutrophication 1850–2006. Ambio 41: 534–548.CrossRefGoogle Scholar
  21. HELCOM. Ministerial Declaration: Taking further action to implement the Baltic Sea Action Plan—Reaching good environmental status for a healthy Baltic Sea (online). HELCOM: Copenhagen, 2013a.Google Scholar
  22. HELCOM. HELCOM HUB—Technical Report on the HELCOM Underwater Biotope and habitat classification. Baltic Sea Environmental Proceedings 139, 2013b.Google Scholar
  23. HELCOM. Red List of Baltic Sea underwater biotopes, habitats and biotope complexes. Baltic Sea Environmental Proceedings 138, 2013c.Google Scholar
  24. Hietanen, S., A.O. Laine, and K. Lukkari. 2007. The complex effects of the invasive polychaetes Marenzelleria spp. on benthic nutrient dynamics. Journal of Experimental Marine Biology and Ecology 352: 89–102.CrossRefGoogle Scholar
  25. Isaev, A.V., T.R. Eremina, V.A. Ryabchenko, and O.P. Savchuk. 2016. Model estimates of the impact of bioirrigation activity of Marenzelleria spp. on the Gulf of Finland ecosystem in a changing climate. Journal of Marine Systems.  https://doi.org/10.1016/j.jmarsys.2016.08.005.CrossRefGoogle Scholar
  26. Karlson, K., S. Hulth, K. Ringdahl, and R. Rosenberg. 2005. Experimental recolonisation of Baltic Sea reduced sediments: Survival of benthic macrofauna and effects on nutrient cycling. Marine Ecology Progress Series 294: 35–49.CrossRefGoogle Scholar
  27. Karlson, A.M.L., G. Almqvist, K.E. Skora, and M. Appelberg. 2007. Indications of competition between non-indigenous round goby and native flounder in the Baltic Sea. ICES Journal of Marine Science 64: 479.CrossRefGoogle Scholar
  28. Karlson, A.M., J. Näslund, S.B. Rydén, and R. Elmgren. 2011. Polychaete invader enhances resource utilization in a species-poor system. Oecologia 166: 1055–1065.CrossRefGoogle Scholar
  29. Kauppi, L., A. Norkko, and J. Norkko. 2015. Large-scale species invasion into a low-diversity system: Spatial and temporal distribution of the invasive polychaetes Marenzelleria spp. in the Baltic Sea. Biological Invasions 17: 2055–2074.CrossRefGoogle Scholar
  30. Kauppi, L., J. Norkko, J. Ikonen, and A. Norkko. 2017. Seasonal variability in ecosystem functions: Quantifying the contribution of invasive species to nutrient cycling in coastal ecosystems. Marine Ecology Progress Series 572: 193–207.CrossRefGoogle Scholar
  31. Kauppi, L., A. Norkko, and J. Norkko. 2018. Seasonal population dynamics of the invasive polychaete genus Marenzelleria spp. in contrasting soft-sediment habitats. Journal of Sea Research 131: 46–60.CrossRefGoogle Scholar
  32. Kotta, J., H. Orav, and E. Sandberg-Kilpi. 2001. Ecological consequence of the introduction of the polychaete Marenzelleria cf. viridis into a shallow-water biotope of the northern Baltic Sea. Journal of Sea Research 46: 273–280.CrossRefGoogle Scholar
  33. Lehtoranta, J., and A.-S. Heiskanen. 2003. Dissolved iron:phosphate ratio as an indicator of phosphate release to oxic water of the inner and outer coastal Baltic Sea. Hydrobiologia 492: 69–84.  https://doi.org/10.1023/a:1024822013580.CrossRefGoogle Scholar
  34. Leipe, T., F. Tauber, H. Vallius, J. Virtasalo, S. Uścinowicz, N. Kowalski, S. Hille, S. Lindgren, et al. 2011. Particulate organic carbon (POC) in surface sediments of the Baltic Sea. Geo-Marine Letters 31: 175–188.CrossRefGoogle Scholar
  35. Leppäkoski, E., and S. Olenin. 2000. Non-native species and rates of spread: Lessons from the brackish Baltic Sea. Biological Invasions 2: 151–163.  https://doi.org/10.1023/a:1010052809567.CrossRefGoogle Scholar
  36. Liaw, A., and M. Wiener. 2002. Classification and regression by randomForest. R News 2: 18–22.Google Scholar
  37. Maes, J., B. Egoh, L. Willemen, C. Liquete, P. Vihervaara, J.P. Schägner, B. Grizzetti, E.G. Drakou, et al. 2012. Mapping ecosystem services for policy support and decision making in the European Union. Ecosystem Services 1: 31–39.CrossRefGoogle Scholar
  38. Maximov, A., E. Bonsdorff, T. Eremina, L. Kauppi, A. Norkko, and J. Norkko. 2015. Context-dependent consequences of Marenzelleria spp. (Spionidae: Polychaeta) invasion for nutrient cycling in the Northern Baltic Sea. Oceanologia 57: 342–348.  https://doi.org/10.1016/j.oceano.2015.06.002.CrossRefGoogle Scholar
  39. Norkko, J., D.C. Reed, K. Timmermann, A. Norkko, B.G. Gustafsson, E. Bonsdorff, C.P. Slomp, J. Carstensen, et al. 2012. A welcome can of worms? Hypoxia mitigation by an invasive species. Global Change Biology 18: 422–434.CrossRefGoogle Scholar
  40. Norling, K. Ecosystem functions in benthos: Importance of macrofaunal bioturbation and biodiversity for mineralization and nutrient fluxes. PhD-Thesis, Department of Marine Ecology, University of Gothenburg, Sweden, 2007.Google Scholar
  41. Norling, K., R. Rosenberg, S. Hulth, A. Grémare, and E. Bonsdorff. 2007. The importance of functional biodiversity and species specific traits of benthic fauna for ecosystem functions in marine sediments. Marine Ecology Progress Series 332: 11–23.CrossRefGoogle Scholar
  42. Quinn, G.P., and M.J. Keough. 2002. Experimental design and data analysis for biologists. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  43. Quintana, C.O., E. Kristensen, and T. Valdemarsen. 2013. Impact of the invasive polychaete Marenzelleria viridis on the biogeochemistry of sandy marine sediments. Biogeochemistry 115: 95–109.CrossRefGoogle Scholar
  44. R Core Team. 2014. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  45. Reed, D.C., C.P. Slomp, and B.G. Gustafsson. 2011. Sedimentary phosphorus dynamics and the evolution of bottom-water hypoxia: A coupled benthic–pelagic model of a coastal system. Limnology and Oceanography 56: 1075–1092.CrossRefGoogle Scholar
  46. Renz, J.R., and S. Forster. 2013. Are similar worms different? A comparative tracer study on bioturbation in the three sibling species Marenzelleria arctia, M. viridis, and M. neglecta from the Baltic Sea. Limnology and Oceanography 58: 2046–2058.CrossRefGoogle Scholar
  47. Renz, J.R., and S. Forster. 2014. Effects of bioirrigation by the three sibling species of Marenzelleria spp. on solute fluxes and porewater nutrient profiles. Marine Ecology Progress Series 505: 145–159.CrossRefGoogle Scholar
  48. Sarda, R., I. Valiela, and K. Foreman. 1995. Life cycle, demography, and production of Marenzelleria viridis in a salt-marsh of southern New England. Journal of the Marine Biological Association of the United Kingdom 75: 725–738.CrossRefGoogle Scholar
  49. Saunders, M.E., and G.W. Luck. 2016. Limitations of the ecosystem services versus disservices dichotomy. Conservation Biology.  https://doi.org/10.1111/cobi.12740.CrossRefGoogle Scholar
  50. Urban-Malinga, B., J. Warzocha, and M. Zalewski. 2013. Effects of the invasive polychaete Marenzelleria spp. on benthic processes and meiobenthos of a species-poor brackish system. Journal of Sea Research 80: 25–34.CrossRefGoogle Scholar
  51. Viitasalo-Frösén, S., A.O. Laine, and M. Lehtiniemi. 2009. Habitat modification mediated by motile surface stirrers versus semi-motile burrowers: Potential for a positive feedback mechanism in a eutrophied ecosystem. Marine Ecology Progress Series 376: 21–32.CrossRefGoogle Scholar
  52. Viktorsson, L., N. Ekeroth, M. Nilsson, M. Kononets, and P.O.J. Hall. 2013. Phosphorus recycling in sediments of the central Baltic Sea. Biogeosciences 10: 3901–3916.CrossRefGoogle Scholar
  53. Virnstein, R.W. 1977. The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay. Ecology 58: 1200–1217.CrossRefGoogle Scholar
  54. Wager, S. randomForestCI: Confidence intervals for random forests. R package version 1.0.0. 2016.Google Scholar
  55. Wager, S., T. Hastie, and B. Efron. 2014. Confidence intervals for random forests: The jackknife and the infinitesimal jackknife. Journal of Machine Learning Research 15: 1625–1651.Google Scholar
  56. Winkler, H.M., and L. Debus. Is the polychaete Marenzelleria viridis an important food item for fish. In Proceedings of the 13th symposium of the Baltic marine biologists, 1996, 147–151.Google Scholar
  57. Zettler, L., D. Daunys, J. Kotta, and A. Bick. 2002. History and success of an invasion into the Baltic Sea: The polychaete Marenzelleria cf. viridis, development and strategies. In Invasive aquatic species of Europe. Distribution, impacts and management, ed. E. Leppäkoski, S. Gollasch, and S. Olenin, 66–75. Dordrecht: Kluwer Academic Publishers.CrossRefGoogle Scholar

Copyright information

© Royal Swedish Academy of Sciences 2018

Authors and Affiliations

  1. 1.AquaBiota Water ResearchStockholmSweden
  2. 2.Department of EconomicsSwedish University of Agricultural EconomicsUppsalaSweden
  3. 3.Swedish Agency for Marine and Water ManagementGöteborgSweden

Personalised recommendations