Epiphyte-cover on seagrass (Zostera marina L.) leaves impedes plant performance and radial O2 loss from the below-ground tissue

Frontiers in Marine Science

Volumn 2, Issue AUG, 2015, Pages

  Brodersen, Kasper E ^a   Lichtenberg, Mads ^b   Paz, Laura Carlota ^c   Kühl, Michael ^a,b  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

Diffusive boundary layer; Epiphyte cover; Light; Microenvironment; Oxic microshield; Radial O2 loss

Indexed keywords

EID: 85008685941     PISSN: None     EISSN: 22967745     Source Type: Journal    
DOI: 10.3389/fmars.2015.00058     Document Type: Article

References (57)

1. Armstrong, W. (1979). Aeration in Higher Plants. London: Academic Press
2. Barnabas, A. D. (1996). Casparian band-like structures in the root hypodermis of some aquatic angiosperms. Aquat. Bot. 55, 217-225. doi: 10.1016/S0304-3770(96)01072-8
3. Binzer, T., Borum, J., and Pedersen, O. (2005). Flow velocity affects internal oxygen conditions in the seagrass Cymodocea nodosa. Aquat. Bot. 83, 239-247. doi: 10.1016/j.aquabot.2005.07.001
4. Borum, J. (1983). "The quantitative role of macrophytes, epiphytes, and phytoplankton under different nutrient conditions in Roskilde Fjord, Denmark," in Proceedings of the International Symposium on Aquatic Macrophytes (Nijmegen), 35-40
5. Borum, J., Pedersen, O., Greve, T. M., Frankovich, T. A., Zieman, J. C., Fourqurean, J. W., et al. (2005). The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. J. Ecol. 93, 148-158. doi: 10.1111/j.1365-2745.2004.00943.x
6. Borum, J., Sand-Jensen, K., Binzer, T., Pedersen, O., and Greve, T. (2006). "Oxygen movement in seagrasses," in Seagrasses: Biology, Ecology and Conservation, eds A. W. D. Larkum, J. R. Orth, and C. M. Duarte (Dordrecht; Berlin: Springer), 255-270
7. Brodersen, K. E., Nielsen, D. A., Ralph, P. J., and Kühl, M. (2014). A split flow chamber with artificial sediment to examine the below-ground microenvironment of aquatic macrophytes. Mar. Biol. 161, 2921-2930. doi: 10.1007/s00227-014-2542-3
8. Brodersen, K. E., Nielsen, D. A., Ralph, P. J., and Kühl, M. (2015). Oxic microshield and local pH enhancement protects Zostera muelleri from sediment derived hydrogen sulphide. New Phytol. 205, 1264-1276. doi: 10.1111/nph.13124
9. Burkholder, J. M., Tomasko, D. A., and Touchette, B. W. (2007). Seagrasses and eutrophication. J. Exp. Mar. Biol. Ecol. 350, 46-72. doi: 10.1016/j.jembe.2007.06.024
10. 2 contingent on epiphytic algae: indirect effects can overwhelm direct effects. Oecologia 176, 871-882. doi: 10.1007/s00442-014-3054-z
11. Dennison, W. J., Orth, R. J., Moore, K. A., Stevenson, J. C., Carter, V., Kollar, S., et al. (1993). Assessing water quality with submerged aquatic vegetation. Bioscience 43, 86-94. doi: 10.2307/1311969
12. Drake, L. A., Dobbs, F. C., and Zimmerman, R. C. (2003). Effects of epiphyte load on optical properties and photosynthetic potential of the seagrasses Thalassia testudinum Banks ex König and Zostera marina L. Limnol. Ocenogr. 48, 456-463. doi: 10.4319/lo.2003.48.1_part_2.0456
13. Duarte, C. M. (1991). Seagrass depth limits. Aquat. Bot. 40, 363-377. doi: 10.1016/0304-3770(91)90081-F
14. Duarte, C. M. (2001). "Seagrass ecosystems," in Encyclopedia of Biodiversity, Vol 5, ed S. L. Leven (San Diego, CA: Academic Press), 254-268. doi: 10.1016/B0-12-226865-2/00241-8
15. Duarte, C. M., Middelburg, J. J., and Caraco, N. (2005). Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2, 1-8. doi: 10.5194/bg-2-1-2005
16. Eghbal, M. A., Pennefather, P. S., and O'Brien, P. J. (2004). H2S cytotoxicity mechanism involves reactive oxygen species formation and mitochondrial depolarisation. Toxicology 203, 69-76. doi: 10.1016/j.tox.2004.05.020
17. Finster, K., Thomsen, T. R., and Ramsing, N. B. (2001). Desulfomusa hansenii gen. nov., sp. nov., a novel marine propionate-degrading, sulfate-reducing bacterium isolated from Zostera marina roots. Int. J. Syst. Evol. Microbiol. 51, 2055-2061. doi: 10.1099/00207713-51-6-2055
18. Frederiksen, M. S., and Glud, R. N. (2006). Oxygen dynamics in the rhizosphere of Zostera marina: a two-dimensional planar optode study. Limnol. Oceanogr. 51, 1072-1083. doi: 10.4319/lo.2006.51.2.1072
19. Frederiksen, M. S., Holmer, M., Borum, J., and Kennedy, H. (2006). Temporal and spatial variation of sulfide invasion in eelgrass (Zostera marina) as reflected by its sulfur isotopic composition. Limnol. Oceanogr. 51, 2308-2318. doi: 10.4319/lo.2006.51.5.2308
20. Goodman, J. L., Moore, K. A., and Dennison, W. C. (1995). Photosynthetic responses of eelgrass (Zostera marina L.) to light and sediment sulfide in a shallow barrier island lagoon. Aquat. Bot. 50, 37-47. doi: 10.1016/0304-3770(94)00444-Q
21. Greve, T. M., Borum, J., and Pedersen, O. (2003). Meristematic oxygen variability in eelgrass (Zostera marina). Limnol. Oceanogr. 48, 210-216. doi: 10.4319/lo.2003.48.1.0210
22. Grieshaber, M. K., and Völkel, S. (1998). Animal adaptations for tolerance and exploitation of poisonous sulfide. Annu. Rev. Physiol. 60, 33-53. doi: 10.1146/annurev.physiol.60.1.33
23. Holmer, M., and Bondgaard, E. J. (2001). Photosynthetic and growth response of eelgrass to low oxygen and high sulfide concentrations during hypoxic events. Aquat. Bot. 70, 29-38. doi: 10.1016/S0304-3770(00)00142-X
24. Holmer, M., Frederiksen, M., and Møllegaard, H. (2005). Sulfur accumulation in eelgrass (Zostera marina) and effect of sulfur on eelgrass growth. Aquat. Bot. 81, 367-379. doi: 10.1016/j.aquabot.2004.12.006
25. Holmer, M., and Hasler-Sheetal, H. (2014). Sulfide intrusion in seagrasses assessed by stable sulfur isotopes-a synthesis of current results. Front. Mar. Sci. 1:64. doi: 10.3389/fmars.2014.00064
26. Jensen, S. I., Kühl, M., Glud, R. N., Jørgensen, L. B., and Prieme, A. (2005). Oxic microzones and radial oxygen loss from roots of Zostera marina. Mar. Ecol. Prog. Ser. 293, 49-58. doi: 10.3354/meps293049
27. Jørgensen, B. B. (1982). Mineralization of organic matter in the sea bed-the role of sulfate reduction. Nature 296, 643-645. doi: 10.1038/296643a0
28. Jørgensen, B. B., and Des Marais, D. J. (1990). The diffusive boundary layer of sediments: oxygen microgradients over a microbial mat. Limnol. Oceanogr. 35, 1343-1355. doi: 10.4319/lo.1990.35.6.1343
29. Jørgensen, B. B., and Postgate, J. R. (1982). Ecology of the bacteria of the Sulfur cycle with special reference to anoxic oxic interface environments. Philos. Trans. R. Soc. Lond. B Biol. Sci. 298, 543-561. doi: 10.1098/rstb.1982.0096
30. Jørgensen, B. B., and Revsbech, N. P. (1985). Diffusive boundary layers and the oxygen uptake of sediments and detritus. Limnol. Oceanogr. 30, 111-122. doi: 10.4319/lo.1985.30.1.0111
31. Kim, Y. K., Kim, S. H., and Lee, K. S. (2015). Seasonal growth responses of the seagrass Zostera marina under severely diminished light conditions. Estuar. Coasts 38, 558-568. doi: 10.1007/s12237-014-9833-2
32. 2 dynamics around the rhizome and roots of seagrasses. Environ. Sci. Technol. 49, 2286-2292. doi: 10.1021/es505734b
33. Kühl, M., and Jørgensen, B. B. (1994). The light-field of microbenthic communities-radiance distribution and microscale optics of sandy coastal sediments. Limnol. Oceanogr. 39, 1368-1398. doi: 10.4319/lo.1994.39.6.1368
34. Lamers, L. P., Govers, L. L., Janssen, I. C., Geurts, J. J., Van der Welle, M. E., Van Katwijk, M. M., et al. (2013). Sulfide as a soil phytotoxin-a review. Front. Plant Sci. 4:268. doi: 10.3389/fpls.2013.00268
35. Lassen, C., Ploug, H., and Jørgensen, B. B. (1992). A fiberoptic scalar irradiance microsensor-application for spectral light measurements in sediments. FEMS Microbiol. Ecol. 86, 247-254. doi: 10.1111/j.1574-6968.1992.tb04816.x
36. Maberly, S. C. (2014). The fitness of the environments of air and water for photosynthesis, growth, reproduction and dispersal of photoautotrophs: an evolutionary and biogeochemical perspective. Aquat. Bot. 118, 4-13. doi: 10.1016/j.aquabot.2014.06.014
37. Nielsen, J. T., Liesack, W., and Finster, K. (1999). Desulfovibrio zosterae sp. nov., a new sulphate reducer isolated from surface-sterilized roots of the seagrass Zostera marina. Int. J. Syst. Evol. Microbiol. 49, 859-865
38. Orth, R. J., Carruthers, T. J., Dennison, W. C., Duarte, C. M., Fourqurean, J. W., Heck, K. L., et al. (2006). A global crisis for seagrass ecosystems. Bioscience 56, 987-996. doi: 10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2
39. Pedersen, M. F., Nejrup, L. B., Pedersen, T. M., and Frederiksen, S. (2014). Sub canopy light conditions only allow low annual net productivity of epiphytic algae on kelp Laminaria hyperborea. Mar. Ecol. Prog. Ser. 516, 163-176. doi: 10.3354/meps11019
40. Pedersen, O., Binzer, T., and Borum, J. (2004). Sulphide intrusion in eelgrass (Zostera marina L.). Plant Cell Environ. 27, 595-602. doi: 10.1111/j.1365-3040.2004.01173.x
41. Pedersen, O., Borum, J., Duarte, C. M., and Fortes, M. D. (1998). Oxygen dynamics in the rhizosphere of Cymodocea rotundata. Mar. Ecol. Prog. Ser. 169, 283-288. doi: 10.3354/meps169283
42. Pérez-Pérez, M. E., Lemaire, S. D., and Crespo, J. L. (2012). Reactive oxygen species and autophagy in plants and algae. Plant Physiol. 160, 156-164. doi: 10.1104/pp.112.199992
43. Plus, M., Deslous-Paoli, J.-M., and Dagault, F. (2003). Seagrass (Zostera marina L.) bed recolonisation after anoxia-induced full mortality. Aquat. Bot. 77, 121-134. doi: 10.1016/S0304-3770(03)00089-5
44. Ralph, P. J., Durako, M. J., Enriquez, S., Collier, C. J., and Doblin, M. A. (2007). Impact of light limitation on seagrasses. J. Exp. Mar. Biol. Ecol. 350, 176-193. doi: 10.1016/j.jembe.2007.06.017
45. Raun, A. L., and Borum, J. (2013). Combined impact of water column oxygen and temperature on internal oxygen status and growth of Zostera marina seedlings and adult shoots. J. Exp. Mar. Biol. Ecol. 441, 16-22. doi: 10.1016/j.jembe.2013.01.014
46. Raven, J. A., and Scrimgeour, C. M. (1997). The influence of anoxia on plants of saline habitats with special reference to the Sulfur cycle. Ann. Bot. 79, 79-86. doi: 10.1093/oxfordjournals.aob.a010309
47. Revsbech, N. P. (1989). An oxygen microsensor with a guard cathode. Limnol. Oceanogr. 34, 474-478. doi: 10.4319/lo.1989.34.2.0474
48. Richardson, S. L. (2006). Response of epiphytic foraminiferal communities to natural eutrophication in seagrass habitats off Man O'War Cay, Belize. Mar. Ecol. 27, 404-416. doi: 10.1111/j.1439-0485.2006.00096.x
49. Robblee, M. B., Barber, T. R., Carlson, P. R. Jr., Durako, M. J., Fourqurean, J. W., Muehlstein, L. K., et al. (1991). Mass mortality of the tropical seagrass Thalassia testudinum in Florida Bay (USA). Mar. Ecol. Prog. Ser. 71, 297-299
50. Sand-Jensen, K. (1977). Effect of epiphytes on eelgrass photosynthesis. Aquat. Bot. 3, 55-63. doi: 10.1016/0304-3770(77)90004-3
51. Sand-Jensen, K., and Borum, J. (1991). Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquat. Bot. 41, 137-175. doi: 10.1016/0304-3770(91)90042-4
52. Seddon, S., Connolly, R., and Edyvane, K. S. (2000). Large-scale seagrass dieback in northern Spencer Gulf, South Australia. Aquat. Bot. 66, 297-310. doi: 10.1016/S0304-3770(99)00080-7
53. Spilling, K., Titelman, J., Greve, T. M., and Kühl, M. (2010). Microsensor measurements of the external and internal microenvironment of Fucus vesiculosus (Phaeophyceae). J. Phycol. 46, 1350-1355. doi: 10.1111/j.1529-8817.2010.00894.x
54. Steen-Knudsen, O. (2002). Biological Membranes: Theory of Transport, Potentials and Electric Impulses. Cambridge, UK: Cambridge University Press
55. Webb, W. L., Newton, M., and Starr, D. (1974). Carbon-dioxide exchange of Alnus-rubra-mathematical-model. Oecologia 17, 281-291. doi: 10.1007/BF00345747
56. 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. doi: 10.2307/1353211
57. Zimmerman, R. C., and Alberte, R. S. (1996). Effect of light/dark transition on carbon translocation in eelgrass Zostera marina seedlings. Mar. Ecol. Prog. Ser. 136, 305-309. doi: 10.3354/meps136305