Hydrogen sulfide intrusion in seagrasses from Shark Bay, Western Australia
Marion L. Cambridge A D , Matthew W. Fraser A , Marianne Holmer B , John Kuo C and Gary A. Kendrick A
+ Author Affiliations
- Author Affiliations
A School of Plant Biology and The UWA Oceans Institute, The University of Western Australia, Crawley, WA 6009, Australia.
B Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark.
C Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, WA 6009, Australia.
D Corresponding author. Email: marion.cambridge@uwa.edu.au
Marine and Freshwater Research 63(11) 1027-1038 https://doi.org/10.1071/MF12022
Submitted: 26 January 2012 Accepted: 21 June 2012 Published: 26 November 2012
Abstract
Sulfides in sediments and hydrogen sulfide (H2S) intrusion in plant tissues were investigated for six species of seagrass in Shark Bay, Western Australia, at two sites with elevated salinities of 42 and 45 psu. H2S intrusion ranged from <20% to 100% in roots and rhizomes, indicating a high degree of sulfide intrusion in some cases, although this did not vary consistently between larger, long-lived species and smaller, less persistent species. There were significant differences in accumulation of total sulfur (TS) among species. Anatomy of rhizomes and roots showed species-specific differences in aerenchyma, the air channels that allow oxygen to diffuse down to the roots and sediments, and tissues with thickened cell walls that could present a barrier to diffusion of H2S, suggesting that morphology may influence sulfide intrusion and sulfur accumulation. Sulfide concentrations in seagrass sediments were far lower in Shark Bay than in Florida Bay, a subtropical embayment where sulfide toxicity has been implicated in seagrass dieback. Despite significant H2S intrusion into tissues of some Shark Bay seagrasses, there was no evidence of any deleterious effects in the current conditions.
Additional keywords: δ34S, hypersalinity, H2S, sulfide pools, sulfur accumulation.
References
Armstrong, J., and Armstrong, W. (2005). Rice: sulphide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Annals of Botany 96, 625–638.| Rice: sulphide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGitLbM&md5=bb7ff1141496cd6ea87f9071c0be097eCAS |
Armstrong, J., Afreen-Zobayed, F., and Armstrong, W. (1996). Phragmites die-back: sulphide- and acetic acid-induced bud and root death, lignifications, and blockages within aeration and vascular systems. New Phytologist 134, 601–614.
| Phragmites die-back: sulphide- and acetic acid-induced bud and root death, lignifications, and blockages within aeration and vascular systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXls1Oguw%3D%3D&md5=9f070832c6eb1ae17f9a4d1fa5aede54CAS |
Berg, P., and Mcglathery, K. M. (2001). A high-resolution pore water sampler for sandy sediments. Limnology and Oceanography 46, 203–210.
| A high-resolution pore water sampler for sandy sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFKjt7c%3D&md5=c522154d063117e965216af907720aa4CAS |
Borum, J., Pedersen, O., Greve, T. M., Francovich, T. A., Zieman, J. C., Fourqurean, J. W., and Madden, C. J. (2005). The potential role of plant oxygen and sulfide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. Journal of Ecology 93, 148–158.
| The potential role of plant oxygen and sulfide dynamics in die-off events of the tropical seagrass, Thalassia testudinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvVCksro%3D&md5=e111e7c18810fb5dd0eae70ec0db21ccCAS |
Calleja, M. L., Marba, N., and Duarte, C. M. (2007). The relationship between seagrass (Posidonia oceanica) decline and sulfide porewater concentration in carbonate sediments. Estuarine, Coastal and Shelf Science 73, 583–588.
| The relationship between seagrass (Posidonia oceanica) decline and sulfide porewater concentration in carbonate sediments.Crossref | GoogleScholarGoogle Scholar |
Carlson, P. R., Yarbro, L. A., and Barber, T. R. (1994). Relationship of sediment sulfide to mortality of Thalassia testudinum in Florida Bay. Bulletin of Marine Science 54, 733–746.
Chambers, R. M., Fourqurean, J. W., Macko, S. A., and Hoppenot, R. (2001). Biogeochemical effects of iron availability on primary producers in a shallow marine carbonate environment. Limnology and Oceanography 46, 1278–1286.
| Biogeochemical effects of iron availability on primary producers in a shallow marine carbonate environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnsVSktLg%3D&md5=5174ffb09472e571e4f0214bb1190b85CAS |
Cline, J. D. (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnology and Oceanography 14, 454–458.
| Spectrophotometric determination of hydrogen sulfide in natural waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1MXksFegu70%3D&md5=f1e652f1bdb368b6c120c5993ae5ef48CAS |
Colmer, T. D. (2003). Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment 26, 17–36.
| Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKrtLs%3D&md5=f318699aec07076942a922ef47cac3daCAS |
Connell, E. L., Colmer, T. D., and Walker, D. I. (1999). Radial oxygen loss from intact roots of Halophila ovalis as a function of distance behind the root tip and shoot illumination. Aquatic Botany 63, 219–228.
| Radial oxygen loss from intact roots of Halophila ovalis as a function of distance behind the root tip and shoot illumination.Crossref | GoogleScholarGoogle Scholar |
Fossing, H., and Jørgensen, B. B. (1989). Measurement of bacterial sulfate reduction in sediments: evaluation of a single-step chromium reduction method. Biogeochemistry 8, 205–222.
| Measurement of bacterial sulfate reduction in sediments: evaluation of a single-step chromium reduction method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXht1ClurY%3D&md5=bf70727c3111440960e938dd3ba1b140CAS |
Frederiksen, M. S., Holmer, M., Borum, J., and Kennedy, H. (2006). Temporal and spatial variation of sulphide invasion in eelgrass (Zostera marina) as reflected by its sulfur isotopic composition. Limnology and Oceanography 51, 2308–2318.
| Temporal and spatial variation of sulphide invasion in eelgrass (Zostera marina) as reflected by its sulfur isotopic composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOju7fN&md5=f40b5d35b5e080115f250f715ef757a3CAS |
Frederiksen, M. S., Holmer, M., Diaz-Almela, E., Marba, N., and Duarte, C. M. (2007). Sulfide invasion in the seagrass Posidonia oceanica at Mediterranean fish farms: assessment using stable sulfur isotopes. Marine Ecology Progress Series 345, 93–104.
| Sulfide invasion in the seagrass Posidonia oceanica at Mediterranean fish farms: assessment using stable sulfur isotopes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhtrfP&md5=591343893691143e380deaebeedcc88aCAS |
Greve, T. M., Borum, J., and Pedersen, O. (2003). Meristematic oxygen variability in eelgrass (Zostera marina). Limnology and Oceanography 48, 210–216.
| Meristematic oxygen variability in eelgrass (Zostera marina).Crossref | GoogleScholarGoogle Scholar |
Halun, Z., Terrados, J., Borum, J., Kamp-Nielsen, L., Duarte, C. M., and Fortes, M. D. (2002). Experimental evaluation of the effects of siltation-derived changes in sediment conditions on the Philippine seagrass Cymodocea rotundata. Journal of Experimental Marine Biology and Ecology 279, 73–87.
| Experimental evaluation of the effects of siltation-derived changes in sediment conditions on the Philippine seagrass Cymodocea rotundata.Crossref | GoogleScholarGoogle Scholar |
Holmer, M., and Bondgaard, E. J. (2001). Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events. Aquatic Botany 70, 29–38.
| Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsVKkt78%3D&md5=a78e356f557e3146602e4bdbde16b157CAS |
Holmer, M., and Kendrick, G. A. (2012). High sulfide intrusion in five temperate seagrasses growing under contrasting sediment conditions. Estuaries and Coasts , .
| High sulfide intrusion in five temperate seagrasses growing under contrasting sediment conditions.Crossref | GoogleScholarGoogle Scholar |
Holmer, M., and Nielsen, R. M. (2007). Effects of filamentous algal mats on sulfide invasion in eelgrass (Zostera marina). Journal of Experimental Marine Biology and Ecology 353, 245–252.
| Effects of filamentous algal mats on sulfide invasion in eelgrass (Zostera marina).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlGgtLnK&md5=6c3dbc53131c6fda3471237faa50f2d1CAS |
Holmer, M., Duarte, C. M., and Marba, N. (2003). Sulfur cycling and seagrass (Posidonia oceanica) status in carbonate sediments. Biogeochemistry 66, 223–239.
| Sulfur cycling and seagrass (Posidonia oceanica) status in carbonate sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Chtb0%3D&md5=06174e5346b5b33d120889f0555bf7baCAS |
Holmer, M., Duarte, C. M., and Marba, N. (2005a). Iron additions reduce sulfate reduction rates and improve seagrass growth on organic-enriched carbonate sediments. Ecosystems 8, 721–730.
| Iron additions reduce sulfate reduction rates and improve seagrass growth on organic-enriched carbonate sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVylurnL&md5=14be2d6498f268240a3cb068cb6fd9c2CAS |
Holmer, M., Frederiksen, M. S., and Mollegaard, H. (2005b). Sulfur accumulation in eelgrass (Zostera marina) and effect of sulfur on eelgrass growth. Aquatic Botany 81, 367–379.
| Sulfur accumulation in eelgrass (Zostera marina) and effect of sulfur on eelgrass growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktVOnu78%3D&md5=2099ac38083fde6c05fa84678d9de87aCAS |
Holmer, M., Pedersen, O., Krause-Jensen, D., Olesen, B., Petersen, M. H., Schopmeyer, S., Koch, M., Lomstein, B. A., and Jensen, H. S. (2009). Sulfide intrusion in the tropical seagrasses Thalassia testudinum and Syringodium filiforme. Estuarine, Coastal and Shelf Science 85, 319–326.
| Sulfide intrusion in the tropical seagrasses Thalassia testudinum and Syringodium filiforme.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSjsbvO&md5=23c94f6037031b6039a777f93dd9ce87CAS |
Kilminster, K. L., Walker, D. I., Thompson, P. A., and Raven, J. A. (2008). Changes in growth, internode distance and nutrient concentrations of the seagrass Halophila ovalis with exposure to sediment sulfide. Marine Ecology Progress Series 361, 83–91.
| Changes in growth, internode distance and nutrient concentrations of the seagrass Halophila ovalis with exposure to sediment sulfide.Crossref | GoogleScholarGoogle Scholar |
Koch, M. S., and Erskine, J. M. (2001). Sulfide as a phytotoxin to the tropical seagrass Thalassia testudinum: interactions with light, salinity and temperature. Journal of Experimental Marine Biology and Ecology 266, 81–95.
| Sulfide as a phytotoxin to the tropical seagrass Thalassia testudinum: interactions with light, salinity and temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXoslWhu7g%3D&md5=d74ea16e7f71c83c055212ede2e0db8cCAS |
Koch, M. S., Benz, R. E., and Rudnick, D. T. (2001). Solid-phase phosphorus pools in highly organic carbonate sediments of northeastern Florida Bay. Estuarine, Coastal and Shelf Science 52, 279–291.
| Solid-phase phosphorus pools in highly organic carbonate sediments of northeastern Florida Bay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsF2itbo%3D&md5=c6fd3a2107ac9b9880629f88d5f27eefCAS |
Koch, M. S., Schopmeyer, S. A., Nielsen, O. I., Kyhn-Hansen, C., and Madden, C. J. (2007a). Conceptual model of seagrass die-off in Florida Bay: links to biogeochemical processes. Journal of Experimental Marine Biology and Ecology 350, 73–88.
| Conceptual model of seagrass die-off in Florida Bay: links to biogeochemical processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSjsrfN&md5=993030c35ecf1149377bac0a9763a272CAS |
Koch, M. S., Schopmeyer, S. A., Kyhn-Hansen, C., and Madden, C. J. (2007b). Synergistic effects of high temperature and sulfide on tropical seagrass. Journal of Experimental Marine Biology and Ecology 341, 91–101.
| Synergistic effects of high temperature and sulfide on tropical seagrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVKjtg%3D%3D&md5=cb3094f411d522b47e4cf04658db0160CAS |
Kuo, J., Takuro Shibuno, T., Kanamoto, Z., and Noro, T. (2001). Halophila ovalis (R.Br.) Hook. f. from a submarine hot spring in southern Japan. Aquatic Botany 70, 329–335.
| Halophila ovalis (R.Br.) Hook. f. from a submarine hot spring in southern Japan.Crossref | GoogleScholarGoogle Scholar |
Pedersen, O., Binzer, T., and Borum, J. (2004). Sulfide intrusion in eelgrass (Zostera marina L.). Plant, Cell & Environment 27, 595–602.
| Sulfide intrusion in eelgrass (Zostera marina L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkvF2ls7o%3D&md5=1294837ba0817dc7b0ec1acfeeb40c16CAS |
Pulich, W. M. (1989). Effects of rhizosphere macronutrients and sulfide levels on the growth physiology of Halodule wrightii Aschers. and Ruppia maritima L. s.l. Journal of Experimental Marine Biology and Ecology 127, 69–80.
| Effects of rhizosphere macronutrients and sulfide levels on the growth physiology of Halodule wrightii Aschers. and Ruppia maritima L. s.l.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltFCgsbc%3D&md5=19751d695b2349e6422f75a97bfecd1aCAS |
R Development Core Team (2012). R: A Language and Environment for Statistical Computing (Version 2.13.1). R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org [accessed 28 September 12]
Raven, J. A., and Scrimgeour, C. M. (1997). The influence of anoxia on plants of saline habitats with special reference to the sulphur cycle. Annals of Botany 79, 79–86.
| The influence of anoxia on plants of saline habitats with special reference to the sulphur cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhtlWrs7Y%3D&md5=d9923a585574b3ce95a6495e69f1e446CAS |
Robblee, M. B., Barber, T. R., Carlson, P. R., Durako, M. J., Fourqurean, J. W., Muehlstein, L. K., Porter, D., Yarbro, L. A., Zieman, R. T., and Zieman, J. C. (1991). Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay. Marine Ecology Progress Series 71, 297–299.
| Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay.Crossref | GoogleScholarGoogle Scholar |
Roberts, D. G., McComb, A. J., and Kuo, J. (1984). The structure and continuity of the lacunar system of the seagrass Halophila ovalis (R.Br.) Hook f. (Hydrocharitaceae). Aquatic Botany 18, 377–388.
| The structure and continuity of the lacunar system of the seagrass Halophila ovalis (R.Br.) Hook f. (Hydrocharitaceae).Crossref | GoogleScholarGoogle Scholar |
Roberts, D. G., McComb, A. J., and Kuo, J. (1985). Root development in the seagrass Halophila ovalis (R.Br.) Hook. f. (Hydrocharitaceae), with particular reference to root lacunae. New Phytologist 100, 25–36.
| Root development in the seagrass Halophila ovalis (R.Br.) Hook. f. (Hydrocharitaceae), with particular reference to root lacunae.Crossref | GoogleScholarGoogle Scholar |
Ruiz-Halpern, S., Macko, S., and Fourqurean, J. W. (2008). The effects of manipulation of sedimentary iron and organic matter on sediment biogeochemistry and seagrasses in a subtropical carbonate environment. Biogeochemistry 87, 113–126.
| The effects of manipulation of sedimentary iron and organic matter on sediment biogeochemistry and seagrasses in a subtropical carbonate environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjslSqtL4%3D&md5=0a95de15b9e937ca631b81d64fb3fa23CAS |
Stookey, L. L. (1970). Ferrozine – A new spectrophotometric reagent for iron. Analytical Chemistry 42, 779–781.
| Ferrozine – A new spectrophotometric reagent for iron.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3cXkt1WjtL8%3D&md5=88a79ed725ee432c1411bb9f236c0bfdCAS |
Zhang, J. Z., Fischer, C. J., and Ortner, P. B. (2004). Potential availability of sedimentary phosphorus to sediment resuspension in Florida Bay. Global Biogeochemical Cycles 18, GB4008.
| Potential availability of sedimentary phosphorus to sediment resuspension in Florida Bay.Crossref | GoogleScholarGoogle Scholar |
Zieman, J. C., Fourqurean, J. W., and Frankovich, T. A. (1999). Seagrass die-off in Florida Bay: long term trends in abundance and growth of turtle grass, Thalassia testudinum. Estuaries 22, 460–470.
| Seagrass die-off in Florida Bay: long term trends in abundance and growth of turtle grass, Thalassia testudinum.Crossref | GoogleScholarGoogle Scholar |
