Vulnerability of macronutrients to the concurrent effects of enhanced temperature and atmospheric pCO2 in representative shelf sea sediment habitats

Biogeochemistry

Volumn 135, Issue 1-2, 2017, Pages 89-102

  Godbold, Jasmin A ^a   Hale, Rachel ^a   Wood, Christina L ^a   Solan, Martin ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Biodiversity; Bioturbation; Macronutrients; Multiple stressors; Ocean acidification; Organic carbon

Indexed keywords

ABUNDANCE; BIODIVERSITY; BIOGEOCHEMISTRY; BIOTURBATION; CARBON DIOXIDE; CLIMATE CHANGE; COMMUNITY STRUCTURE; ENVIRONMENTAL CONDITIONS; ENVIRONMENTAL STRESS; FUNCTIONAL ROLE; HIGH TEMPERATURE; MICROBIAL COMMUNITY; OCEAN ACIDIFICATION; ORGANIC CARBON; SEAWATER; SHELF SEDIMENT; SPECIES RICHNESS; VULNERABILITY;

ATLANTIC OCEAN; CELTIC SEA;

INVERTEBRATA;

EID: 85020664934     PISSN: 01682563     EISSN: 1573515X     Source Type: Journal    
DOI: 10.1007/s10533-017-0340-y     Document Type: Article

References (92)

1. Alsterberg C, Eklöf JS, Gamfeldt L et al (2013) Consumers mediate the effects of experimental ocean acidification and warming on primary producers. Proc Natl Acad Sci USA 110:8603–8608
2. Anthony KRN, Kline DI, Diaz-Pulido G et al (2008) Ocean acidification causes bleaching and productivity loss in coral reef builders. Proc Natl Acad Sci USA 105:17442–17446. doi:10.1073/pnas.0804478105
3. Bates NR, Orchowska MI, Garley R et al (2013) Summertime calcium carbonate undersaturation in shelf waters of the western Arctic Ocean—how biological processes exacerbate the impact of ocean acidification. Biogeosciences 10:5281–5309
4. Beman JM, Chow CE, King AL et al (2011) Global declines in oceanic nitrification rates as a consequence of ocean acidification. Proc Natl Acad Sci USA 108:208–213
5. Botto F, Valiela I, Iribarne O et al (2005) Impact of burrowing crabs on C and N sources, control, and transformations in sediments and food webs of SW Atlantic estuaries. Mar Ecol Prog Ser 293:155–164
6. Braeckman U, Van Colen C, Guilini K et al (2014) Empirical evidence reveals seasonally dependent reduction in nitrification in coastal sediments subjected to near future ocean acidification. PLoS ONE 9:e108153. doi:10.1371/journal.pone.0108153
7. Bulling MT, Hicks N, Murray L et al (2010) Marine biodiversity-ecosystem functions under uncertain environmental futures. Phil Trans R Soc Biol 365:2107–2116
8. Burdige DJ (2006) Geochemistry of marine sediments. Princeton University Press, New Jersey
9. Busch DS, McElhany P (2016) Estimates of the direct effect of seawater pH on the survival rate of species groups in the California current ecosystem. PLoS ONE 11(8):e0160669. doi:10.1371/journal.pone.0160669
10. 2. Deep-Sea Res II 56:578–581
11. Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80
12. Comeau S, Jeffree R, Teyssie J-L et al (2010) Response of the Arctic pteropod Limacina helicina to pro- jected future environmental conditions. PLoS ONE 5:e11362.
13. Cowan JLW, Boynton WR (1996) Sediment-water oxygen and nutrient exchanges along the longitudinal axis of Chesapeake Bay: seasonal patterns, controlling factors and ecological significance. Estuaries 19:562–580
14. Crook ED, Kroeker KJ, Potts DC et al (2016) Recruitment and succession in a tropical benthic community in response to in-situ ocean acidification. PLoS ONE 11:e0146707. doi:10.1371/journal.pone.0146707
15. 4—in synthetic sea water from 273.15 to 318.15 K. J Chem Thermodyn 22:113–127. doi:10.1016/0021-9614(90)90074-Z
16. Dickson AG (2010) The carbon dioxide system in seawater: equilibrium chemistry and measurements In U Riebesell, VJ Fabry, L Hansson, J-P Gattuso (eds) Guide to best practices for ocean acidification research and data reporting, 260 pp. Luxembourg: Publications Office of the European Union
17. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Res A 34:1733–1743. doi:10.1016/0198-0149(87)90021-5
18. Dickson AG, Sabine CL, Christian JR (eds) (2007) Guide to best practices for ocean CO2 measurements, vol. 3, 191 pp. PICES Special Publication
19. Downing JA (1997) Marine nitrogen:phosphorus stoichiometry and the global N: P cycle. Biogeochemistry 37:237–252
20. 2-carbonic acid system chemistry in permeable carbonate reef sands. Mar Chem 185:48–64. doi:10.1016/j.marchem.2016.04.004
21. Eklöf JS, Havenhand JN, Alsterberg A et al (2015) Community-level effects of rapid experimental warming and consumer loss outweigh effects of rapid ocean acidification. Oikos 124:1040–1049. doi:10.1111/oik.01544
22. Elser JJ, Bracken ME, Cleland EE et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142
23. 2 exposure in the cold-water coral Lophelia pertusa. Glob Chang Biol 18:843–853
24. Forster S, Glud RN, Gundersen JK et al (1999) In situ study of bromide tracer and oxygen flux in coastal sediment. Estuar Coast Shelf Sci 49:813–827. doi:10.1006/ecss.1999.0557
25. Gachter R, Muller B (2003) Why the phosphorus retention of lakes does not necessarily depend on the oxygen supply to their sediment surface. Limnol Oceanogr 48:929–933
26. 2 vent system: winners and losers among closely related species. Mar Ecol Progr Ser 550:121–134
27. Gattuso JP, Hansson L (2011) Ocean acidification: background and history. In: Gattuson J-P, Hansson L (eds) Ocean acidification. Oxford University Press, Oxford, pp 1–17
28. Gazeau F, van Rijswijk P, Pozzato L et al (2014) Impacts of ocean acidification on sediment processes in shallow waters of the Arctic ocean. PLoS ONE 9:e94068. doi:10.1371/journal.pone.0094068
29. Ghalambor CK, McKay JK, Carroll SP et al (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407
30. Gilbertson WW, Solan M, Prosser JI (2012) Differential effects of microorganism-invertebrate interactions on benthic nitrogen cycling. FEMS Microbiol Ecol 82:11–22
31. Godbold JA, Solan M (2009) Relative importance of biodiversity and the abiotic environment in mediating an ecosystem process. Mar Ecol Prog Ser 396:273–282
32. Godbold JA, Solan M (2013) Long-term effects of warming and ocean acidification are modified by seasonal variation in species responses and environmental conditions. Phil Trans R Soc B 368:20130186. doi:10.1098/rstb.2013.0186
33. Hale R, Calosi P, McNeill L et al (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674. doi:10.1111/j.1600-0706.2010.19469.x
34. Hale R, Mavrogordato MN, Tolhurst TJ et al (2014) Characterizations of how species mediate ecosystem properties require more comprehensive functional effect descriptors. Sci Rep 4:6463. doi:10.1038/srep06463
35. Hale R, Godbold JA, Sciberras M et al (2017) Mediation of macronutrients and carbon by post-disturbance shelf sea sediment communities. Biogeochemistry. doi:10.1007/s10533-017-0350-9
36. Hall-Spencer JM, Rodolfo-Metalpa R, Martin S et al (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99. doi:10.1038/nature07051
37. Hansen K, King GM, Kristensen E (1996) Impact of the soft shell clam Mya arenaria on sulphate reduction in an intertidal sediment. Aquat Microb Ecol 10:181–194
38. Harpole WS, Ngai JT, Cleland EE et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862. doi:10.1111/j.1461-0248.2011.01651.x
39. Hedges JI, Keil RG (1995) Preservation of extremely oxygen-sensitive organic materials such as pigments and unsaturated lipids. Mar Chem 49:81–115
40. Hicks N, Bulling MT, Solan M et al (2011) Impact of biodiversity- climate futures on primary production and metabolism in a model benthic estuarine system. BMC Ecol 11:7. doi:10.1186/1472-6785-11-7
41. Huesemann MH, Skillman AD, Crecelius EA (2002) The inhibition of marine nitrification by ocean disposal of carbon dioxide. Mar Poll Bull 44:142–148
42. 2-enriched ocean. Oceanography 22:128–145
43. IPCC (2014) Climate Change 2014: Synthesis Report. In: Core Writing Team, R.K. Pachauri and L.A. Meyer (eds.) Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland
44. Jickells T (1998) Nutrient biogeochemistry of the coastal zone. Science 281:217–221
45. Johnson KS, Chavez FP, Friederich GE (1999) Continental-shelf sediment as a primary source of iron for coastal phytoplankton. Nature 398:697–700
46. Johnson MD, Price NN, Smith JE (2014) Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2:e411. doi:10.7717/peerj.411
47. Kim K (2016) Review of inorganic nitrogen transformations and effect of global climate change on inorganic nitrogen cycling in ocean ecosystems. Ocean Sci J 51(2):159–167
48. Kitidis V, Laverock B, McNeill L et al (2011) Impact of ocean acidification on benthic and water column ammonia oxidation. Geophys Res Lett 38:L21603. doi:10.1029/2011GL049095
49. Kitidis V, Tait K, Nunes J et al (2017) Seasonal benthic nitrogen cycling in a temperate shelf sea; the Celtic Sea. Biogeochemistry. doi:10.1007/s10533-017-0311-3
50. Kroeker KJ, Kordas RL, Crim R et al (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Chang Biol 19:1884–1896. doi:10.1111/gcb.12179
51. Kroeker KJ, Gaylord B, Hill TM et al (2014) The role of temperature in determining species’ vulnerability to ocean acidification: a case study using Mytilus galloprovincialis. PLoS ONE 9:e100353
52. Laverock B, Smith CJ, Tait K et al (2010) Bioturbating shrimp alter the structure and diversity of bacterial communities in coastal marine sediments. ISME J 12:1531–1544. doi:10.1038/ismej.2010.86
53. Laverock B, Gilbert JA, Tait K et al (2011) Bioturbation: impact on the marine nitrogen cycle. Biochem Soc Trans 39:315–320
54. Laverock B, Kitidis V, Tait K et al (2013) Bioturbation determines the response of benthic ammonia-oxidizing microorganisms to ocean acidification. Phil Trans R Soc B 368:20120441
55. Li Q, Wang X, Kan D et al (2012) Enrichment of phosphate on ferrous iron phases during bio-reduction of ferrihydrite. Int J Geosci 3:314–320
56. Lohrer AM, Thrush SF, Gibbs MM (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–1095. doi:10.1038/nature03042
57. Maire O, Merchant JN, Bulling M et al (2010) Indirect effects of non-lethal predation on bivalve activity and sediment reworking. J Exp Mar Biol Ecol 395:30–36
58. Mayor DJ, Thornton B, Hay S et al (2012) Resource quality affects carbon cycling in deep-sea sediments. ISME J 6:1740–1748. doi:10.1038/ismej.2012.14
59. McCulloch M, Falter J, Trotter J et al (2012) Coral resilience to ocean acidification and global warming through pH up-regulation. Nat Clim Chang 2:623–627. doi:10.1038/nclimate1473
60. 2 and temperature on an intertidal meiobenthic community. J Exp Mar Biol Ecol 469:44–56
61. Mehrbach C, Culberson CH, Hawley JE et al (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907. doi:10.4319/lo.1973.18.6.0897
62. 2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS ONE 6:e24223. doi:10.1371/journal.pone.0024223
63. Micheli F, Halpern BS (2005) Low functional redundancy in coastal marine assemblages. Ecol Lett 8:391–400. doi:10.1111/j.1461-0248.2005.00731.x
64. Oksanen, J, Blanchet GF, Kindt R et al (2016) ‘vegan’—Community Ecology Package
65. Ouellette D, Desrosiers G, Gagne JP 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
66. Patrick WH Jr, Khalid RA (1974) Phosphate release and sorption by soils and sediments: effect of aerobic and anaerobic conditions. Sci New Ser 186:53–55
67. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322:690–692. doi:10.1126/science.1163156
68. Przeslawski R, Ahyong S, Byrne M et al (2008) Beyond corals and fish: the effects of climate change on non-coral benthic invertebrates of tropical reefs. Glob Chang Biol 14:2773–2795
69. Queirós AM, Birchenough SNR, Bremner J et al (2013) A bioturbation classification of European marine infaunal invertebrates. Ecol Evol 3:3958–3985. doi:10.1002/ece3.769
70. 2 and experimental stress. Mar Ecol Prog Ser 509:153–170. doi:10.3354/meps10861
71. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
72. Robador A, Bruchert V, Jorgensen BB (2009) The impact of temperature change on the activity and community composition of sulfate-reducing bacteria in arctic versus temperate marine sediments. Environ Microbiol 11:1692–1703
73. Robbins LL, Hansen ME, Kleypas JA, Meylan SC (2010) CO2calc—a user-friendly seawater carbon calculator for Windows, Max OS X, and iOS (iPhone). US Geological Survey Open-File Report 2010–1280
74. Rocha C (2008) Sandy sediments as active biogeochemical reactors: compound cycling in the fast lane. Aquatic Microb Ecol 53:119–127
75. Roden EE, Edmonds JW (1997) Phosphate mobilization in iron-rich anaerobic sediments: microbial Fe(III) oxide reduction versus iron-sulfide formation. Arch Hydrobiol 139:347–378
76. Rodolfo-Metalpa R, Houlbrèque F, Tambutté É et al (2011) Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature 1:308–312
77. 2 and temperature on an intertidal harpacticoid copepod community. ICES J Mar Sci
78. Sciberras M, Tait K, Brochain G et al (2017) Community mediation on shelf-sea benthic nitrogen cycling following bottom trawling and organic enrichment. Biogeochemistry (submitted)
79. Solan M, Wigham BD, Hudson IR et al (2004a) In situ quantification of bioturbation using time-lapse fluorescent sediment profile imaging (f-SPI), luminophore tracers and model simulation. Mar Ecol Prog Ser 271:1–12. doi:10.3354/meps271001
80. Solan M, Cardinale BJ, Downing AL et al (2004b) Extinction and ecosystem function in the marine benthos. Science 306:1177–1180
81. 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
82. Tait K, Laverock B, Shaw J et al (2013) Minor impact of ocean acidification to the composition of the active microbial community in an Arctic sediment. Environ Microbiol Rep 5:851–860
83. 2. Estuar Coast 37:724–735
84. 2 levels in a mesocosm study. Biogeosciences 5:669–678
85. Tatters AO, Roleda MY, Schnetzer A et al (2013) Short-and long-term conditioning of a temperate marine diatom community to acidification and warming. Phil Trans R Soc B 368:20120437
86. Thompson CEL, Silburn B, Williams ME et al (2017) An approach for the identification of exemplar sites for scaling up targeted field observations of benthic biogeochemistry in heterogeneous environments. Biogeochemistry (submitted)
87. Thomsen MS, Garcia C, Bolam S, Parker R, Godbold JA, Solan M (2017) Consequences of biodiversity loss diverge from expectation due to post-extinction compensatory responses. Sci Rep 7:43695
88. Voss M, Bange HW, Dippner JW, Middelburg JJ, Montoya JP, Ward B (2013) The marine nitrogen cycle: recent discoveries, uncertainties and the potential relevance of climate change. Philos Trans R Soc B 368:1621. doi:10.1098/rstb.2013.0121
89. Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: procedures, patterns and problems. Glob Chang Biol 18:1491–1498
90. 2 induced seawater acidification on infaunal diversity and sediment nutrient fluxes. Mar Ecol Prog Ser 379:59–75
91. 2 on animal mediated ecosystem function: the modification of sediment nutrient fluxes by burrowing urchins. Mar Poll Bull 73:416–427. doi:10.1016/j.marpolbul.2012.11.008
92. Yool A, Popova EE, Anderson TR (2013) MEDUSA-2.0: an intermediate complexity biogeochemical model of the marine carbon cycle for climate change and ocean acidification studies. Geosci Model Dev 6:1767–1811. doi:10.5194/gmd-6-1767-2013