Empirical evidence reveals seasonally dependent reduction in nitrification in coastal sediments subjected to near future ocean acidification

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Braeckman, Ulrike ^a   Van Colen, Carl ^a   Guilini, Katja ^a   Van Gansbeke, Dirk ^a   Soetaert, Karline ^b   Vincx, Magda ^a   Vanaverbeke, Jan ^a  

^a GHENT UNIVERSITY   (Belgium)

^b ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIFICATION; ARTICLE; BENTHOS; BIODIVERSITY; CLIMATE CHANGE; COASTAL WATERS; MACROFAUNA; NITRIFICATION; NONHUMAN; OXYGEN CONSUMPTION; PH; PHYTOPLANKTON; SEA; SEASONAL VARIATION; SEDIMENT; WINTER; CHEMISTRY; METABOLISM; SEASON;

CARBONIC ACID DERIVATIVE; NITROGEN OXIDE; OXYGEN; PIGMENT; SEA WATER;

CARBONATES; CLIMATE CHANGE; GEOLOGIC SEDIMENTS; HYDROGEN-ION CONCENTRATION; NITRIFICATION; NITROGEN OXIDES; OXYGEN; PIGMENTS, BIOLOGICAL; SEASONS; SEAWATER;

EID: 84908052465     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108153     Document Type: Article

References (65)

1. Solomon S, Qin D, Manning M, Chen Z, Marquis M, et al. (2007) The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernemental panel on climate change. Cambridge Univ. Press, Cambridge, UK, and New York.
2. Brewer PG (2009) A changing ocean seen with clarity. Proc Natl Acad Sci 106: 12213-12214.
3. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425: 365.
4. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, et al. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686.
5. Wootton JT, Pfister CA, Forester JD (2008) Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc Natl Acad Sci 105: 18848-18853.
6. Provoost P, van Heuven S, Soetaert K, Laane R, Middelburg JJ (2010) Long-term record of pH in the Dutch coastal zone: a major role for eutrophication-induced changes. Biogeosciences 7: 3869-3878.
7. Andersson AJ, Mackenzie FT, Gattuso J-P (2011) Effects of ocean acidification on benthic processes, organisms, and ecosystems. Ocean acidification. Oxford University Press, Oxford. pp. 122-153.
8. Pörtner H-O, Gutowska M, Ishimatsu A, Lucassen A, Melzner F, et al. (2011) Effects of ocean acidification on nektonic organisms. Ocean acidification. Oxford University Press, Oxford. pp. 154-175.
9. Riebesell U, Tortell PD (2011) Effects of ocean acidification on pelagic organisms and ecosystems. Ocean acidification. Oxford University Press, Oxford. pp. 99-112.
10. Widdicombe S, Spicer JI, Kitidis V (2011) Effects of ocean acidification on sediment fauna. Ocean acidification. Oxford University Press, Oxford. pp. 113-122.
11. Kroeker KJ, Micheli F, Gambi MC, Martz TR (2011) Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc Natl Acad Sci 108: 14515-14520.
12. Gehlen M, Gruber N, Gangsto R, Bopp L, Oschlies A (2011) Biogeochemical consequences of ocean acidification and feedbacks to the earth system. Ocean acidification. Oxford University Press, Oxford. pp. 230-248.
13. 2-enriched ocean. Oceanography 22.
14. Voss M, Bange HW, Dippner JW, Middelburg JJ, Montoya JP, et al. (2013) The marine nitrogen cycle: recent discoveries, uncertainties and the potential relevance of climate change. Philos Trans R Soc B Biol Sci 368: 20130121.
15. Huesemann MH, Skillman AD, Crecelius EA (2002) The inhibition of marine nitrification by ocean disposal of carbon dioxide. Mar Pollut Bull 44: 142-148.
16. Beman JM, Chow C-E, King AL, Feng Y, Fuhrman JA, et al. (2011) Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc Natl Acad Sci 108: 208-213.
17. Kitidis V, Laverock B, McNeill LC, Beesley A, Cummings D, et al. (2011) Impact of ocean acidification on benthic and water column ammonia oxidation. Geophys Res Lett 38: L21603.
18. Laverock B, Kitidis V, Tait K, Gilbert JA, Osborn AM, et al. (2013) Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification. Philos Trans R Soc B Biol Sci 368: 20120441.
19. 2-induced seawater acidification on the burrowing activity of Nereis virens and sediment nutrient flux. Mar Ecol Prog Ser 341: 111-122.
20. 2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Mar Ecol Prog Ser 379: 59-75.
21. Wood HL, Widdicombe S, Spicer JI (2009) The influence of hypercapnia and the infaunal brittlestar Amphiura filiformis on sediment nutrient flux- will ocean acidification affect nutrient exchange? Biogeosciences 6: 2015-2024.
22. Godbold JA, Solan M (2013) Long-term effects of warming and ocean acidification are modified by seasonal variation in species responses and environmental conditions. Philos Trans R Soc B Biol Sci 368: 20130186.
23. Murray F, Widdicombe S, McNeill CL, Solan M (2013) Consequences of a simulated rapid ocean acidification event for benthic ecosystem processes and functions. Mar Pollut Bull 73: 435-442.
24. 2 on animal mediated ecosystem function: The modification of sediment nutrient fluxes by burrowing urchins. Mar Pollut Bull 73: 416-427.
25. Gazeau F, van Rijswijk P, Pozzato L, Middelburg JJ (2014) Impacts of Ocean Acidification on Sediment Processes in Shallow Waters of the Arctic Ocean. Plos One 9: e94068.
26. Ouellette D, Desrosiers G, Gagne JP, Gilbert F, Poggiale JC, et al. (2004) Effects of temperature on in vitro sediment reworking processes by a gallery biodiffusor, the polychaete Neanthes virens. Mar Ecol Prog Ser 266: 185-193.
27. Maire O, Duchene JC, Rosenberg R, de Mendonca J, Gremare A (2006) Effects of food availability on sediment reworking in Abra ovata and A. nitida. Mar Ecol Prog Ser 319: 135-153.
28. Braeckman U, Provoost P, Gribsholt B, Van Gansbeke D, Middelburg JJ, et al. (2010) Role of macrofauna functional traits and density in biogeochemical fluxes and bioturbation. Mar Ecol Prog Ser 399: 173-186.
29. Soetaert K, Herman PMJ, Middelburg JJ, Heip C, Smith CL, et al. (2001) Numerical modelling of the shelf break ecosystem: reproducing benthic and pelagic measurements. Deep-Sea Res Part II 48: 3141-3177.
30. Lancelot C, Spitz Y, Gypens N, Ruddick K, Becquevort S, et al. (2005) Modelling diatom and Phaeocystis blooms and nutrient cycles in the Southern Bight of the North Sea: the MIRO model. Mar Ecol Prog Ser 289: 63-78.
31. Van Oevelen D, Soetaert K, Franco MA, Moodley L, van IJzerloo L, et al. (2009) Organic matter input and processing in two contrasting North Sea sediments: insights from stable isotope and biomass data. Mar Ecol Prog Ser 380: 19-32.
32. Huettel M, Rusch A (2000) Transport and degradation of phytoplankton in permeable sediment. Limnol Oceanogr 45: 534-549.
33. Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110: C09S04.
34. Riebesell U, Fabry VJ, Hansson L, Gattuso JP (2010) Guide to best practices for ocean acidification research and data reporting. Luxembourg: Publications Office of the European Union. 260 p.
35. 2 measurements. Available: http://aquaticcommons.org/1443/.
36. 2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge, TN.
37. Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, et al. (2004) Extinction and ecosystem function in the marine benthos. Science 306: 1177-1180.
38. Queirós AM, Birchenough SNR, Bremner J, Godbold JA, Parker RE, et al. (2013) A bioturbation classification of European marine infaunal invertebrates. Ecol Evol 13: 3958-3985.
39. Wright SW, Jeffrey SW (1997) High-resolution HPLC system for chlorophylls and carotenoids of marine phytoplankton. Jeffrey Sw Mantoura Rfc Wright Sw Eds Phytoplankton Pigments Ocean Guid Mod Methods Unesco Paris Pp 327-341.
40. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press New York.
41. Braeckman U, Foshtomi MY, Van Gansbeke D, Meysman F, Soetaert K, et al. (2014) Variable importance of macrofaunal functional biodiversity for biogeochemical cycling in temperate coastal sediments. Ecosystems 17: 720-737.
42. West B, Welch KB, Galecki AT (2006) Linear Mixed Models: A Practical Guide Using Statistical Software. Taylor & Francis. 382 p.
43. Pinheiro JC, Bates D (2009) Mixed-Effects Models in S and S-PLUS. Springer. 538 p.
44. Zuur A, Ieno EN, Walker N (2009) Mixed Effects Models and Extensions in Ecology with R. Springer. 580 p.
45. Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press.
46. Kuhn M, Weston S, Wing J, Forester J, Thaler T (2013) Contrast: A collection of contrast methods. R package version 0.19. Available at http://CRAN.Rproject.org/package=contrast.
47. Clarke KR, Gorley RN (2006) Primer v6: User Manual/Tutorial. Primer-E Plymouth.
48. Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-E Plymouth.
49. Dashfield SL, Somerfield PJ, Widdicombe S, Austen MC, Nimmo M (2008) Impacts of ocean acidification and burrowing urchins on within-sediment pH profiles and subtidal nematode communities. J Exp Mar Biol Ecol 365: 46-52.
50. 2. Geochim Cosmochim Acta 65: 2677-2690.
51. Jourabchi P, Cappellen PV, Regnier P (2005) Quantitative interpretation of pH distributions in aquatic sediments: A reaction-transport modeling approach. Am J Sci 305: 919-956.
52. 2 and "ocean acidification": Role of high Mg-calcites. Geochim Cosmochim Acta 70: 5814-5830.
53. Suzuki I, Dular U, Kwok SC (1974) Ammonia or Ammonium Ion as Substrate for Oxidation by Nitrosomonas europaea Cells and Extracts. J Bacteriol 120: 556-558.
54. Ward BB (1987) Kinetic studies on ammonia and methane oxidation by Nitrosococcus oceanus. Arch Microbiol 147: 126-133.
55. 2 in Seawater: Equilibrium, Kinetics, Isotopes: Equilibrium, Kinetics, Isotopes. Elsevier. 362 p.
56. Stief P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10: 7829-7846.
57. Laverock B, Tait K, Gilbert J, Osborn A, Widdicombe S (2013) Impacts of bioturbation on temporal variation in bacterial and archaeal nitrogen-cycling gene abundance in coastal sediments. Environ Microbiol Reports 6: 113-121.
58. 2 on the fixed nitrogen inventory of the Western English Channel. J Plankton Res 32: 631-641.
59. Gilbertson WW, Solan M, Prosser JI (2012) Differential effects of microorganism-invertebrate interactions on benthic nitrogen cycling. Fems Microbiol Ecol 82: 11-22.
60. Tait K, Laverock B, Shaw J, Somerfield PJ, Widdicombe S (2013) Minor impact of ocean acidification to the composition of the active microbial community in an Arctic sediment. Environ Microbiol Reports 5: 851-860.
61. 2. Estuaries Coasts: 1-12.
62. Godbold JA, Calosi P (2013) Ocean acidification and climate change: advances in ecology and evolution. Philos Trans R Soc B Biol Sci 368: 20120448.
63. Kemp WM, Sampou P, Caffrey J, Mayer M, Henriksen K, et al. (1990) Ammonium recycling versus denitrification in Chesapeake Bay sediments. Limnol Oceanogr 35: 1545-1563.
64. Lohse L, Malschaert JFP, Slomp CP, Helder W, van Raaphorst W (1993) Nitrogen cycling in North Sea sediments: interaction of denitrification and nitrification in offshore and coastal areas. Mar Ecol Prog Ser 101: 283-283.
65. 2. Environ Sci Technol 46: 10651-10659.