Belowground stressors and long-term seagrass declines in a historically degraded seagrass ecosystem after improved water quality

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Fraser, Matthew W ^a   Kendrick, Gary A ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

HEAVY METAL; SULFIDE;

ALISMATALES; BIOMASS; ECOSYSTEM; ENVIRONMENTAL MONITORING; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; SEDIMENT; WATER QUALITY; WESTERN AUSTRALIA;

ALISMATALES; BIOMASS; ECOSYSTEM; ENVIRONMENTAL MONITORING; GEOLOGIC SEDIMENTS; METALS, HEAVY; PLANT LEAVES; STRESS, PHYSIOLOGICAL; SULFIDES; WATER QUALITY; WESTERN AUSTRALIA;

EID: 85032635232     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-14044-1     Document Type: Article

References (59)

1. Orth, R. et al. A global crisis for seagrass ecosystems. BioScience 56, 987-996 (2006).
2. Cambridge, M. & McComb, A. The loss of seagrasses in Cockburn Sound, Western Australia. I. The time course and magnitude of seagrass decline in relation to industrial development. Aquatic Botany 20, 229-243 (1984).
3. Kendrick, G. A. et al. Changes in seagrass coverage in Cockburn Sound, Western Australia between 1967 and 1999. Aquatic Botany 73, 75-87 (2002).
4. Brodersen, K. E., Nielsen, D. A., Ralph, P. J. & Kuhl, M. Oxic microshield and local pH enhancement protects Zostera muellerifrom sediment derived hydrogen sulphide. New Phytologist 205, 1264-1276 (2014).
5. Pages, A., Welsh, D. T., Robertson, D. & Panther, J. G. Diurnal shifts in co-distributions of sulfide and iron(II) and profiles of phosphate and ammonium in the rhizosphere of Zostera capricorni. Estuarine, Coastal and Shelf Science (2012).
6. Borum, J. et al. Eelgrass fairy rings: sulfide as inhibiting agent. Marine Biology 161, 351-358 (2013).
7. Greve, T. M., Krause-Jensen, D., Rasmussen, M. B. & Christensen, P. B. Means of rapid eelgrass (Zostera marina L.) recolonisation in former dieback areas. Aquatic Botany 82, 143-156 (2005).
8. Borum, J. et al. 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 (2005).
9. Cambridge, M., Chiffings, A., Brittan, C., Moore, L. & McComb, A. The loss of seagrass in Cockburn Sound, Western Australia II. Possible causes of seagrass decline. Aquatic Botany 24, 269-285 (1986).
10. Cockburn, S. Management Council. State of Cockburn Sound report 2014, 1-24 (2015).
11. Mohring, M. & Rule, M. Long-term trends in the condition of seagrass meadows in Cockburn and Warnbro Sounds. Report prepared for the Cockburn Sound Management Council. 1-94 (2013).
12. Mohring, M. & Rule, M. A Survey of Selected Seagrass Meadows in Cockburn Sound, Owen Anchorage and Warnbro Sound. Data Report prepared for Cockburn Sound Management Council. 1-49 (2014).
13. Frederiksen, M. S., Holmer, M., Diaz-Almela, E., Marba, N. & Duarte, C. M. Sulfide invasion in the seagrass Posidonia oceanica at Mediterranean fish farms: Assessment using stable sulfur isotopes. Marine Ecology Progress Series 345, 93-104 (2007).
14. Pedersen, O., Binzer, T. & Borum, J. Sulphide intrusion in eelgrass (Zostera marina L.). Plant, Cell & Environment 27, 595-602 (2004).
15. Holmer, M., Pedersen, O. & Ikejima, K. Sulfur cycling and sulfide intrusion in mixed southeast Asian tropical seagrass meadows. Botanica Marina 49, 91-102 (2006).
16. Holmer, M. et al. Sulfide intrusion in the tropical seagrasses Thalassia testudinum and Syringodium filiforme. Estuarine, Coastal and Shelf Science 85, 319-326 (2009).
17. Holmer, M. & Kendrick, G. A. High sulfide intrusion in five temperate seagrasses growing under contrasting sediment conditions. Estuaries and Coasts 36, 116-126 (2013).
18. Erskine, J. M. & Koch, M. S. Sulfide effects on Thalassia testudinum carbon balance and adenylate energy charge. Aquatic Botany 67, 275-285 (2000).
19. Marba, N., Calleja, M. L., Duarte, C. M. & Alvarez, E. Iron Additions Reduce Sulfide Intrusion and Reverse Seagrass (Posidonia oceanica) Decline in Carbonate Sediments. Ecosystems 10, 745-756 (2007).
20. Luther, G. W. & Church, T. M. Seasonal cycling of sulfur and iron in porewaters of a Delaware salt marsh. Marine Chemistry (1988).
21. Holmer, M. & Hasler-Sheetal, H. Sulfide intrusion in seagrasses assessed by stable sulfur isotopes-a synthesis of current results. Front. Mar. Sci. 1, 64 (2014).
22. Macinnis-Ng, C. M. O. & Ralph, P. J. Towards a more ecologically relevant assessment of the impact of heavy metals on the photosynthesis of the seagrass, Zostera capricorni. Marine Pollution Bulletin 45, 100-106 (2002).
23. Luy, N., Gobert, S., Sartoretto, S. & Biondo, R. Chemical contamination along the Mediterranean French coast using Posidonia oceanica (L.) Delile above-ground tissues: A multiple trace element study. Ecological Indicators 18, 269-277 (2012).
24. Serrano, O., Mateo, M. A., Renom, P. & Julia, R. Characterization of soils beneath a Posidonia oceanica meadow. Geoderma 185-186, 26-36 (2012).
25. Zhang, C. et al. Effects of sediment geochemical properties on heavy metal bioavailability. Environment International (2014).
26. Bennett, W. W. et al. Inorganic arsenic and iron(II) distributions in sediment porewaters investigated by a combined DGTcolourimetric DET technique. Environ. Chem. 9, 31-40 (2012).
27. Malea, P., Adamakis, I.-D. S. & Kevrekidis, T. Microtubule integrity and cell viability under metal (Cu, Ni and Cr) stress in the seagrass Cymodocea nodosa. Chemosphere 93, 1035-1042 (2013).
28. Cambridge, M. L., Fraser, M. W., Holmer, M., Kuo, J. & Kendrick, G. A. Hydrogen sulfide intrusion in seagrasses from Shark Bay, Western Australia. Marine and Freshwater Research 63, 1027-1038 (2012).
29. Talbot, V. & Chegwidden, A. Cadmium and other heavy metal concentrations in selected biota from Cockburn Sound, Western Australia. Marine and Freshwater Research 33, 779 (1982).
30. Tovar-Sanchez, A., Seron, J., Marba, N., Arrieta, J. M. & Duarte, C. M. Long-term records of trace metal content of western Mediterranean seagrass (Posidonia oceanica) meadows: Natural and anthropogenic contributions. J. Geophys. Res. 115, G02006 (2010).
31. Fraser, M. W., Kendrick, G. A. & Zavala-Perez, A. Drivers of seagrass decline in Cockburn and Warnbro Sound. Report prepared for the Department of Environment Regulation. 1-35 (2016).
32. Environmental Protection Authority. Environmental Quality Criteria Reference Document for Cockburn Sound (2015). 1-108 (2015).
33. Holmer, M., Argyrou, M., Dalsgaard, T. & Danovaro, R. Effects of fish farm waste on Posidonia oceanica meadows: synthesis and provision of monitoring and management tools. Marine Pollution Bulletin 56, 1618-1629 (2008).
34. Lavery, P. S. & McMahon, K. Review of Cockburn Sound SEP Seagrass Monitoring Program (No. CMER 2011-04). Report prepared for the Cockburn Sound Management Council (2011).
35. Fraser, M. W., Statton, J., Hovey, R. K., Laverock, B. & Kendrick, G. Seagrass derived organic matter influences biogeochemistry, microbial communities, and seedling biomass partitioning in seagrass sediments. Plant and Soil #400, 133-146,. https://doi. org/10. 1007/s11104-015-2721-0 (2015).
36. Garcias-Bonet, N., Marba, N., Holmer, M. & Duarte, C. M. Effects of sediment sulfides on seagrass Posidonia oceanica meristematic activity. Marine Ecology Progress Series 372, 1-6 (2008).
37. Fraser, M. W. et al. Extreme climate events lower resilience of foundation seagrass at edge of biogeographical range. Journal of Ecology 102, 1528-1536 (2014).
38. Lee, K. S. & Dunton, K. H. Diurnal changes in pore water sulfide concentrations in the seagrass Thalassia testudinum beds: The effects of seagrasses on sulfide dynamics. Journal of Experimental Marine Biology and Ecology (2000).
39. Holmer, M., Duarte, C. M. & Marba, N. Sulfur cycling and seagrass (Posidonia oceanica) status in carbonate sediments. Biogeochemistry 66, 223-239 (2003).
40. Pedersen, O., Colmer, T. D., Borum, J., Zavala-Perez, A. & Kendrick, G. A. Heat stress of two tropical seagrass species during low tides-impact on underwater net photosynthesis, dark respiration and diel in situ internal aeration. New Phytologist 210, 1207-1218 (2016).
41. Kilminster, K., Forbes, V. & Holmer, M. Ecological Indicators. Ecological Indicators 36, 280-289 (2014).
42. Holmer, M., Duarte, C. M. & Marba, N. Iron additions reduce sulfate reduction rates and improve seagrass growth on organicenriched carbonate sediments. Ecosystems 8, 721-730 (2005).
43. Talbot, V. & Chegwidden, A. Heavy metals in the sediments of Cockburn Sound, Western Australia, and its surrounding areas. Environmental Pollution Series B, Chemical and Physical 5, 187-205 (1983).
44. Leleyter, L., Rousseau, C., Biree, L. & Baraud, F. Comparison of EDTA, HCl and sequential extraction procedures, for selected metals (Cu, Mn, Pb, Zn), in soils, riverine and marine sediments. Journal of Geochemical Exploration 116-117, 51-59 (2012).
45. McCready, S., Birch, G. F. & Taylor, S. E. Extraction of heavy metals in Sydney Harbour sediments using 1M HCl and 0. 05M EDTA and implications for sedimentquality guidelines. Australian Journal of Earth Sciences 50, 249-255 (2003).
46. Heron, G., Crouzet, C. & Bourg, A. Speciation of Fe (II) and Fe (III) in contaminated aquifer sediments using chemical extraction techniques. Environ. Sci. Technol. 28, 1698-1705 (1994).
47. Berner, R. A. Sedimentary pyrite formation: An update. Geochimica et Cosmochimica Acta 48, 650-615 (1984).
48. Rainbow, P. S. Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183-192 (1995).
49. Ralph, P. J. & Burchett, M. D. Photosynthetic response of Halophila ovalis to heavy metal stress. Environmental Pollution (1998).
50. Avelar, M. et al. Iron, cadmium, and chromium in seagrass (Thalassia testudinum) from a coastal nature reserve in karstic Yucatan. Environ Monit Assess 185, 7591-7603 (2013).
51. Malea, P. Uptake of Cadmium and the Effect on Viability of Leaf Cells in the Seagrass Halophila stipulacea (Forsk.) Aschers. Botanica Marina 37 (1994).
52. Ernst, W., Krauss, G. J., Verkleij, J. & Wesenberg, D. Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant, Cell & Environment 31, 123-143 (2008).
53. Skene, D., Ryan, D., Brooke, B. & Smith, J. The Geomorphology and Sediments of Cockburn Sound. Geoscience Australia (2005).
54. Barwick, M. & Maher, W. Biotransference and biomagnification of selenium copper, cadmium, zinc, arsenic and lead in a temperate seagrass ecosystem from Lake Macquarie Estuary, NSW, Australia. Marine Environmental Research 56, 471-502 (2003).
55. Short, F. & Duarte, C. In (eds Short, F. T., Short, C. A. & Coles, R. G.) 155-182 (Global seagrass research methods, 2001).
56. Fourqurean, J. W. et al. Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience 5, 505-509 (2012).
57. Wheal, M. S., Fowles, T. O. & Palmer, L. T. A cost-effective acid digestion method using closed polypropylene tubes for inductively coupled plasma optical emission spectrometry (ICP-OES) analysis of plant essential elements. Anal. Methods 3, 2854-2863 (2011).
58. R Core Team. R Foundation for Statistical Computing. Vienna, Austria. R: A language and environment for statistical computing (2014).
59. Wickham, H. ggplot2: elegant graphics for data analysis. (Springer New York, 2009).