Global warming enhances sulphide stress in a key seagrass species (NW Mediterranean)

Global Change Biology

Volumn 19, Issue 12, 2013, Pages 3629-3639

  García, Rosa ^a   Holmer, Marianne ^b   Duarte, Carlos M ^a,c,d   Marbà, Núria ^a  

^a INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

34S; Climate change; Intrusion; Mortality; Population growth; Seagrass; Sulphide; Temperature; Toxicity

Indexed keywords

CLIMATE CHANGE; GLOBAL WARMING; GREENHOUSE GAS; LEAF; MORTALITY; POPULATION GROWTH; SEA SURFACE TEMPERATURE; SEAGRASS; SEAWATER; SULFIDE; SULFUR ISOTOPE; TOXICITY; WATER DEPTH;

BALEARIC ISLANDS; MEDITERRANEAN SEA; SPAIN;

POSIDONIA OCEANICA;

SEA WATER; SULFIDE;

ALISMATALES; ARTICLE; CHEMISTRY; CLIMATE CHANGE; ENVIRONMENT; GREENHOUSE EFFECT; GROWTH, DEVELOPMENT AND AGING; INTRUSION; MASS SPECTROMETRY; MEDITERRANEAN SEA; METABOLISM; MORTALITY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; POPULATION DYNAMICS; POPULATION GROWTH; SEAGRASS; SEASON; SPAIN; SULPHIDE; TEMPERATURE; TOXICITY; Δ34S;

CLIMATE CHANGE; INTRUSION; MORTALITY; POPULATION GROWTH; SEAGRASS; SULPHIDE; TEMPERATURE; TOXICITY; Δ34S;

ALISMATIDAE; ENVIRONMENT; GLOBAL WARMING; MASS SPECTROMETRY; MEDITERRANEAN SEA; PLANT LEAVES; POPULATION DYNAMICS; SEASONS; SEAWATER; SPAIN; STRESS, PHYSIOLOGICAL; SULFIDES; TEMPERATURE;

EID: 84887486828     PISSN: 13541013     EISSN: 13652486     Source Type: Journal    
DOI: 10.1111/gcb.12377     Document Type: Article

References (68)

1. Arnaud-Haond S, Duarte CM, Diaz-Almela E, Marbà N, Sintes T, Serrao E (2012) Implications of extreme life span in clonal organisms: millenary clones in meadows of the threatened seagrass Posidonia oceanica. PLoS ONE, 7, e30454, doi: 10.1371/journal.pone.0030454.
2. Barrón C, Duarte CM (2009) Dissolved organic matter release in a Posidonia oceanica meadow. Marine Ecology Progress Series, 374, 75-84.
3. Berner RA (1984) Sedimentary pyrite formation: an update. Geochimica et Cosmochimica Acta, 48, 605-615.
4. Borum J, Pedersen O, Greve TM, Frankovich TA, Zieman JC, Fourqurean JW, Madden CJ (2005) The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. Journal of Ecology, 93, 148-158.
5. Borum J, Sand-Jensen K, Binzer T, Pedersen O, Greve TM (2006) Oxygen movement in seagrasses. In: Seagrasses: Biology, Ecology and Conservation (eds Larkum AWD, Orth JR, Duarte CM), pp. 255-270. Springer, the Netherlands.
6. Boudouresque CF, Bernard G, Pergent G, Shili A, Verlaque M (2009) Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review. Botanica Marina, 52, 395-418.
7. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771-1789.
8. Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer Verlag, New York, NY.
9. Burrows MT, Schoeman DS, Buckley LB et al. (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science, 334, 652-655.
10. Cade BS, Noon BR (2003) A gentle introduction to quantile regression for ecologists. Frontiers in Ecology and the Environment, 1, 412-420.
11. Calleja ML, Marbà N, Duarte CM (2007) The relationship between seagrass (Posidonia oceanica) decline and sulfide porewater concentration in carbonate sediments. Estuarine, Coastal and Shelf Science, 73, 583-588.
12. Canfield DE, Thamdrup B (1994) The production of S-34 depleted sulfide during bacterial disproportionation of elemental sulfur. Science, 266, 1973-1975.
13. Carlson PR Jr, Yarbro LA, Barber TR (1994) Relationship of sediment sulfide to mortality of Thalassia testudinum in Florida Bay. Bulletin of Marine Science, 54, 733-746.
14. Coma R, Ribes M, Serrano E, Jiménez E, Salat J, Pascual J (2009) Global warming-enhanced stratification and mass mortality events in the Mediterranean. Proceedings of the National Academy of Sciences of the United States of America, 106, 6176-6181.
15. Diaz-Almela E, Marbà N, Duarte CM (2007) Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records. Global Change Biology, 13, 224-235.
16. Duarte CM (2002) The future of seagrass meadows. Environmental Conservation, 29, 192-206.
17. Duarte CM, Chiscano CL (1999) Seagrass biomass and production: a reassessment. Aquatic Botany, 65, 159-174.
18. Fenchel T, Finlay BJ (1995). Ecology and Evolution in Anoxic Worlds. Oxford University Press, New York, NY.
19. Fernández de Puelles ML, Pinot JM, Valencia J (2003) Seasonal and interannual variability of zooplankton community in waters of Mallorca islands (Balearic Sea, Western Mediterranean): 1994-1999. Oceanologica Acta, 26, 673-686.
20. Fossing H, Jørgensen BB (1989) Measurement of bacterial sulfate reduction in sediments: evaluation of a single-step chromium reduction method. Biogeochemistry, 8, 205-222.
21. Fourqurean JW, Duarte CM, Kennedy H et al. (2012) Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience, 5, 505-509.
22. Frederiksen MS, Glud RN (2006) Oxygen dynamics in the rhizosphere of Zostera marina: A two-dimensional planar optode study. Limnology and Oceanography, 51, 1072-1083.
23. Frederiksen MS, Holmer M, Borum J, Kennedy H (2006) Temporal and spatial variation of sulfide invasion in eelgrass (Zostera marina) as reflected by its sulfur isotopic composition. Limnology and Oceanography, 51, 2308-2318.
24. Gacia E, Duarte CM (2001) Sediment retention by a mediterranean Posidonia oceanica meadow: the balance between deposition and resuspension. Estuarine Coastal and Shelf Science, 52, 505-514.
25. Gacia E, Duarte CM, Middelburg JJ (2002) Carbon and nutrient deposition in a Mediterranean seagrass (Posidonia oceanica) meadow. Limnology and Oceanography, 47, 23-32.
26. García R, Sánchez-Camacho M, Duarte CM, Marbà N (2012) Warming enhances sulphide stress of Mediterranean seagrass (Posidonia oceanica). Estuarine, Coastal and Shelf Science, 113, 240-247.
27. Garcias-Bonet N, Marbà N, Holmer M, Duarte CM (2008) Effects of sediment sulfides on seagrass Posidonia oceanica meristematic activity. Marine Ecology Progress Series, 372, 1-6.
28. Garcias-Bonet N, Arrieta JM, de Santana CN, Duarte CM, Marbà N (2012) Endophytic bacterial community of a Mediterranean marine angiosperm (Posidonia oceanica). Frontiers in Aquatic Microbiology, 3, 1-16.
29. Gobert S, Cambridge ML, Velimirov B (2006) Biology of Posidonia. In: Seagrasses: Biology, Ecology and Conservation (eds Larkum AWD, Orth RJ, Duarte CM), pp. 387-408. Springer, the Netherlands.
30. Goodman JL, Moore KA, Dennison WC (1995) Photosynthetic responses of eelgrass (Zostera marina L.) to light and sediment sulfide in a shallow barrier island lagoon. Aquatic Botany, 50, 37-47.
31. Greve TM, Borum J, Pedersen O (2003) Meristematic oxygen variability in eelgrass (Zostera marina). Limnology and Oceanography, 48, 210-216.
32. Habicht KS, Canfield DE (1997) Sulfur isotope fractionation during bacterial sulfate reduction in organic-rich sediments. Geochimica et Cosmochimica Acta, 61, 5351-5361.
33. Hoegh-Guldberg O, Bruno JF (2010) The impact of climate change on the world's marine ecosystems. Science, 328, 1523-1528.
34. Holmer M, Bondgaard EJ (2001) Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events. Aquatic Botany, 70, 29-38.
35. Holmer M, Kendrick GA (2012) High sulfide intrusion in five temperate seagrasses growing under contrasting sediment conditions. Estuaries and Coasts, 36, 116-126.
36. Holmer M, Nielsen RM (2007) Effects of filamentous algal mats on sulfide invasion in eelgrass (Zostera marina). Journal of Experimental Marine Biology and Ecology, 353, 245-252.
37. Holmer M, Storkholm P (2001) Sulphate reduction and sulphur cycling in lake sediments: a review. Freshwater Biology, 46, 431-451.
38. Holmer M, Duarte CM, Marbà N (2003) Sulfur cycling and seagrass (Posidonia oceanica) status in carbonate sediments. Biogeochemistry, 66, 223-239.
39. Holmer M, Baden S, Boström C, Moksnes PO (2009a) Regional variation in eelgrass (Zostera marina) morphology, production and stable sulfur isotopic composition along the Baltic Sea and Skagerrak coasts. Aquatic Botany, 91, 303-310.
40. Holmer M, Pedersen O, Krause-Jensen D et al. (2009b) Sulfide intrusion in the tropical seagrasses Thalassia testudinum and Syringodium filiforme. Estuarine, Coastal and Shelf Science, 85, 319-326.
41. Holmer M, Marbà N, Lamonte M, Duarte CM (2009c) Deterioration of sediment quality in seagrass meadows (Posidonia oceanica) invaded by macroalgae (Caulerpa sp.). Estuaries and Coasts, 32, 456-466.
42. IPCC (2007) Climate Change 2007: The Physical Science Basis - Summary for Policymakers Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Intergovernmental Panel on Climate Change, Geneva, Switzerland.
43. Jansá J, Fernández de Puelles M, López-Jurado JL, Amengual B, Reñones O, Morillas A (1994) Variación annual e internanual de los factores fisico-químicos generales del medio pelágico de la bahía de Palma (Islas Baleares, España) desde mayo de 1988 hasta mayo de 1992. Informes Técnicos Instituto Español de Oceanografía, 152, 1-83.
44. Jordà G, Marbà N, Duarte CM (2012) Mediterranean seagrass vulnerable to regional climate warming. Nature, 2, 821-824. doi: 10.1038/nclimate1533.
45. Knoblauch C, Jørgensen BB (1999) Effect of temperature on sulphate reduction, growth rate and growth yield in five psychrophilic sulphate-reducing bacteria from Arctic sediments. Environmental Microbiology, 1, 457-467.
46. Koch MS, Schopmeyer SA, Holmer M, Madden CJ, Kyhn-Hansen C (2007) Thalassia testudinum response to the interactive stressors hypersalinity, sulfide and hypoxia. Aquatic Botany, 87, 104-110.
47. Koenker R, Bassett G (1978) Regression quantiles. Econometrica, 46, 33-50.
48. Lelieveld J, Berresheim H, Borrmann S et al. (2002) Global air pollution crossroads over the Mediterranean. Science, 298, 794-799.
49. Marbà N, Duarte CM (1998) Rhizome elongation and seagrass clonal growth. Marine Ecology Progress Series, 174, 269-280.
50. Marbà N, Duarte C (2010) Mediterranean warming triggers seagrass (Posidonia oceanica) shoot mortality. Global Change Biology, 16, 2366-2375.
51. Marbà N, Duarte CM, Cebrian J, Gallegos ME, Olesen B, SandJensen K (1996) Growth and population dynamics of Posidonia oceanica on the Spanish Mediterranean coast: elucidating seagrass decline. Marine Ecology Progress Series, 137, 203-213.
52. Marbà N, Calleja ML, Duarte CM, Álvarez E, Díaz-Almela E, Holmer M (2007) Iron additions reduce sulfide intrusion and reverse seagrass (Posidonia oceanica) decline in carbonate sediments. Ecosystems, 10, 745-756.
53. Mascaró O, Valdemarsen T, Holmer M, Pérez M, Romero J (2009) Experimental manipulation of sediment organic content and water column aeration reduces Zostera marina (eelgrass) growth and survival. Journal of Experimental Marine Biology and Ecology, 373, 26-34.
54. Olsen YS, Sánchez-Camacho M, Marbà N, Duarte CM (2012) Mediterranean seagrass growth and demography responses to experimental warming. Estuaries and Coasts, 35, 1205-1213.
55. Pasqualini V, Pergent-Martini C, Clabaut P, Pergent G (1998) Mapping of Posidonia oceanica using aerial photographs and side scan sonar: application off the Island of Corsica (France). Estuarine Coastal and Shelf Science, 47, 359-367.
56. Pasqualini V, Pergent-Martini C, Pergent G (1999) Environmental impact identification along the Corsican coast (Mediterranean sea) using image processing. Aquatic Botany, 65, 311-320.
57. Pedersen O, Binzer T, Borum J (2004) Sulphide intrusion in eelgrass (Zostera marina L.). Plant, Cell and Environment, 27, 595-602.
58. Povidisa K, Delefosse M, Holmer M (2009) The formation of iron plaques on roots and rhizomes of the seagrass Cymodocea serrulata (R. Brown) Ascherson with implications for sulphide intrusion. Aquatic Botany, 90, 303-308.
59. R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing.Vienna, Austria. ISBN: 3-900051-07-0. Available at: http://www.R-project.org/ (accessed 27 August 2013).
60. Rixen M, Beckers JM, Levitus S et al. (2005) The Western Mediterranean deep water: a proxy for climate change. Geophysical Research Letters, 32, L12608, doi: 10.1029/2005GL022702.
61. Robblee MB, Barber TR, Carlson PR et al. (1991) Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA). Marine Ecology Progress Series, 71, 297-299.
62. Ruiz JM, Romero J (2003) Effects of disturbances caused by coastal constructions on spatial structure, growth dynamics and photosynthesis of the seagrass Posidonia oceanica. Marine Pollution Bulletin, 46, 1523-1533.
63. Schaub BEM, Van Gemerden H (1996) Sulfur bacteria in sediments of two coastal ecosystems: the Bassin d'Arcachon and the Etang du Prévost, France. Hydrobiologia, 329, 199-210.
64. Short FT, Duarte CM (2001) Methods for the measurement of seagrass growth and production. In: Global Seagrass Research Methods (eds Short FT, Coles RG), pp. 155-182. Elsevier, Amsterdam.
65. Solomon S, Qin D, Manning M et al. (2007) Technical Summary. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL), pp. 237-336. Cambridge University Press, Cambridge, UK and New York, NY, USA.
66. Vaquer-Sunyer R, Duarte CM (2008) Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences of the United States of America, 105, 15452-15457.
67. Vaquer-Sunyer R, Duarte CM (2010) Sulfide exposure accelerates hypoxia-driven mortality. Limnology and Oceanography, 55, 1075-1082.
68. Vaquer-Sunyer R, Duarte CM (2011) Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Global Change Biology, 17, 1788-1797.