[en] Posidonia oceanica is the only reported seagrass to produce significant amount of dimethylsulfoniopropionate (DMSP). It is also the largest known producer of DMSP among coastal and inter-tidal higher plants. Here, we studied (i) the weekly to seasonal variability and the depth variability of DMSP and its related compound dimethylsulfoxide (DMSO) in P. oceanica leaves of a non-disturbed meadow in Corsica, France, (ii) the weekly to seasonal variability and the depth variability of DMSP to DMSO concentration to assess the potential of the DMSP:DMSO ratio as indicator of stress, and (iii) the relationships between DMSP, DMSO, and the DMSP:DMSO ratio with potential explanatory variables such as light, temperature, photosynthetic activity (effective quantum yield of photosystem II), and leaf size. The overall average concentrations of organosulfured compounds in P. oceanica leaves were 130 ± 39 μmol.g−1fw for DMSP and 4.9 ± 2.1 μmol.g−1fw for DMSO. Concentrations of DMSP and DMSO in P. oceanica were overall distinctly higher and exhibited a wider range of variations than other marine primary producers such as Spartina alterniflora, phytoplankton communities, epilithic Cyanobacteria and macroalgae. Concentrations of both DMSP and DMSO in P. oceanica leaves decreased from a maximum in autumn to a minimum in summer; they changed little with depth. Potential explanatory variables except the leaf size, i.e., the leaf age were little or not related to measured concentrations. To explain the seasonal pattern of decreasing concentrations with leaf aging, we hypothesized two putative protection functions of DMSP in young leaves: antioxidant against reactive oxygen species and predator-deterrent. The similar variation of the two molecule concentrations over time and with depth suggested that DMSO content in P. oceanica leaves results from oxidation of DMSP. The DMSP:DMSO ratio remained constant around a mean value of 29.2 ± 9.0 μmol:μmol for the non-disturbed harvested meadow regardless of the time of the year, the depth or the leaf size. As suggested for the salt march plant S. alterniflora, we hypothesized the DMSP:DMSO ratio could be considered as indicator of stress in seagrasses exposed to environmental or anthropogenic stressors. More research would now be needed to confirm the functions of DMSP and DMSO in seagrasses and how the DMSP:DMSO ratio will vary under various disturbances.
Research Center/Unit :
Unit of Chemical Oceanography, ULiege FOCUS, ULiege
Disciplines :
Aquatic sciences & oceanology
Author, co-author :
Richir, Jonathan ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Champenois, Willy ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Engels, Guyliann
Abadie, Arnaud ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Gobert, Sylvie ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Lepoint, Gilles ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Silva, João
Santos, Rui
Sirjacobs, Damien ; Université de Liège - ULiège > Département des sciences de la vie > Phylogénomique des eucaryotes
Borges, Alberto ; Université de Liège - ULiège > Département d'astrophys., géophysique et océanographie (AGO) > Chemical Oceanography Unit (AGO)
Language :
English
Title :
A 15-Month Survey of Dimethylsulfoniopropionate and Dimethylsulfoxide Content in Posidonia oceanica
Publication date :
31 January 2020
Journal title :
Frontiers in Ecology and Evolution
eISSN :
2296-701X
Publisher :
Frontiers Media S.A., Switzerland
Volume :
7
Issue :
510
Pages :
1-15
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
DMSP and DMSO in seagrass meadows
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique ULiège - Université de Liège Collectivity of Corsica Agence de l'eau Rhône Méditerranée Corse FCT - Foundation for Science and Technology
Alcoverro T., Manzanera M., Romero J., (1998). Seasonal and age-dependent variability of Posidonia oceanica (L.) Delile photosynthetic parameters. J. Exp. Mar. Bio. Ecol. 230, 1–13. 10.1016/S0022-0981(98)00022-7
Apostolaki E. T., Holmer M., Santinelli V., Karakassis I., (2018). Species-specific response to sulfide intrusion in native and exotic Mediterranean seagrasses under stress. Mar. Environ. Res. 134, 85–95. 10.1016/j.marenvres.2017.12.00629331242
Asher E., Dacey J. W., Ianson D., Peña A., Tortell P. D., (2017). Concentrations and cycling of DMS, DMSP, and DMSO in coastal and offshore waters of the Subarctic Pacific during summer, 2010-2011. J. Geophys. Res. Ocean 122, 3269–3286. 10.1002/2016JC012465
Bay D., (1984). A field study of the growth dynamics and productivity of Posidonia oceanica in Calvi Bay, Corsica, France. Aquat. Bot. 20, 43–64. 10.1016/0304-3770(84)90026-3
Binard M., (2017). Composantes météorologiques de la base de données océanographique RACE de STARESO (Baie de Calvi – Corse). Bull. Soc. Géogr. Liège 68, 37–47. 10.25518/0770-7576.4517
Borges A. V., Champenois W., (2015). Seasonal and spatial variability of dimethylsulfoniopropionate (DMSP) in the Mediterranean seagrass Posidonia oceanica. Aquat. Bot. 125, 72–79. 10.1016/j.aquabot.2015.05.008
Borges A. V., Champenois W., (2017). Preservation protocol for dimethylsulfoniopropionate and dimethylsulfoxide analysis in plant material of the Mediterranean seagrass Posidonia oceanica, and re-evaluation of dimethylsulfoniopropionate leaf content. Aquat. Bot. 143, 8–10. 10.1016/j.aquabot.2017.08.004
Boudouresque C. F., Bernard G., Bonhomme P., Charbonnel E., Meinesz A., Pergent G, et al. (2012). Protection Conservation of Posidonia oceanica Meadows. Tunis: RAMOGE RAC/SPA Publisher.
Boudouresque C. F., Meinesz A., (1982). Découverte de l'herbier de posidonie. Cah. Parc. Natl. Port Cros. 4, 1–79.
Brimblecombe P., Shooter D., (1986). Photo-oxidation of dimethylsulphide in aqueous solution. Mar. Chem. 19, 343–353. 10.1016/0304-4203(86)90055-1
Bullock H. A., Luo H., Whitman W. B., (2017). Evolution of dimethylsulfoniopropionate metabolism in marine phytoplankton and bacteria. Front. Microbiol. 8:637. 10.3389/fmicb.2017.0063728469605
Campagne C. S., Salles J. M., Boissery P., Deter J., (2015). The seagrass Posidonia oceanica: ecosystem services identification and economic evaluation of goods and benefits. Mar. Pollut. Bull. 97, 391–400. 10.1016/j.marpolbul.2015.05.06126028167
Challenger F., Simpson M. I., (1948). Studies on biological methylation. Part, X. I. I. A precursor of the dimethyl sulphide evolved by Polysiphonia fastigiata. Dimethyl-2-carboxyethylsulphonium hydroxide and its salts. J. Chem. Soc. 3, 1591–1597. 10.1039/jr9480001591
Champenois W., Borges A. V., (2012). Seasonal and interannual variations of community metabolism rates of a Posidonia oceanica seagrass meadow. Limnol. Ocean 57, 347–361. 10.4319/lo.2012.57.1.0347
Champenois W., Borges A. V., (2019a). Determination of dimethylsulfoniopropionate and dimethylsulfoxide in Posidonia oceanica leaf tissue. MethodsX 6, 56–62. 10.1016/j.mex.2018.12.01430619727
Champenois W., Borges A. V., (2019b). Inter-annual variations over a decade of primary production of the seagrass Posidonia oceanica. Limnol. Oceanogr. 64, 32–45. 10.1002/lno.11017
Charlson R. J., Lovelock J. E., Andreae M. O., Warren S. G., (1987). Oceanic phytoplancton, atmoshperic sulphur, cloud albedo and climate. Nature 326, 655–661. 10.1038/326655a0
Cook R. D., (1977). Detection of influential observation in linear regression. Technometrics 19, 15–18. 10.1080/00401706.1977.10489493
Dacey J. W. H., King G. M., Lobel P. S., (1994). Herbivory by reef fishes and the production of dimethylsulfide and acrylic acid. Mar. Ecol. Prog. Ser. 112, 67–74. 10.3354/meps112067
Dacey J. W. H., Wakeham S. G., Howes B. L., (1987). Factors controlling emission of dimethylsulphide from salt marshes. Nature 330, 643–645. 10.1038/330643a0
Darmaraki S., Somot S., Sevault F., Nabat P., Narvaez W. D. C., Cavicchia L., et al. (2019). Future evolution of marine heatwaves in the Mediterranean Sea. Clim. Dyn. 53, 1371–1392. 10.1007/s00382-019-04661-z
Dauby P., Poulicek M., (1995). Methods for removing epiphytes from seagrasses: SEM observations on treated leaves. Aquat. Bot. 52, 217–228. 10.1016/0304-3770(95)00500-5
De los Santos C. B., Vicencio-Rammsy B., Lepoint G., Remy F., Bouma T. J., Gobert S., (2016). Ontogenic variation and effect of collection procedure on leaf biomechanical properties of Mediterranean seagrass Posidonia oceanica (L.) Delile. Mar. Ecol. 37, 750–759. 10.1111/maec.12340
Deschaseaux E. S. M., Kiene R. P., Jones G. B., Deseo M. A., Swan H. B., Oswald L., et al. (2014). Dimethylsulphoxide (DMSO) in biological samples: A comparison of the TiCl 3 and NaBH 4 reduction methods using headspace analysis. Mar. Chem. 164, 9–15. 10.1016/j.marchem.2014.05.004
Duarte B., Martins I., Rosa R., Matos A. R., Roleda M. Y., Reusch T. B. H., et al. (2018). Climate change impacts on seagrass meadows and macroalgal forests: An integrative perspective on acclimation and adaptation potential. Front. Mar. Sci. 5:190. 10.3389/fmars.2018.00190
Ferrat L., Pergent-Martini C., Roméo M., (2003). Assessment of the use of biomarkers in aquatic plants for the evaluation of environmental quality: application to seagrasses. Aquat. Toxicol. 65, 187–204. 10.1016/S0166-445X(03)00133-412946618
Fowler J., Cohen L., (1990). Practical Statistics for Field Biology. Chichester: John Wiley & Sons Ltd.
Giraud G., (1979). Sur une méthode de mesure et de comptage des structures foliaires de Posidonia oceanica (Linnaeus) Delile. Bull. Mus. Hist. Nat. Marseille 39, 33–39.
Gobert S., Cambridge M. L., Velimirov B., Pergent G., Lepoint G., Bouquegneau J. M., et al. (2006). “Biology of posidonia,” in Seagrasses: Biology, Ecology and Conservation, eds Larkum A. W. D., Orth R. J., Duarte C. M., (Dordrecht: Springer), 387–408.
Gobert S., Kyramarios M., Lepoint G., Pergent-Martini C., Bouquegneau J., (2003). Variations at different spatial scales of Posidonia oceanica (L.) Delile beds; effects on the physico-chemical parameters of the sediment. Oceanol. Acta 26, 199–207. 10.1016/S0399-1784(02)00009-9
Gobert S., Sartoretto S., Rico-Raimondino V., Andral B., Chery A., Lejeune P., et al. (2009). Assessment of the ecological status of Mediterranean French coastal waters as required by the Water Framework Directive using the Posidonia oceanica Rapid Easy Index: PREI. Mar. Pollut. Bull. 58, 1727–1733. 10.1016/j.marpolbul.2009.06.01219700176
Green T. K., Hatton A. D., (2014). The Claw hypothesis: a new perspective on the role of biogenic sulphur in the regulation of global climate. Oceanogr. Mar. Biol. An. Annu. Rev. 52, 315–336. 10.1201/b17143-7
Hajiboland R., (2014). “Reactive oxygen species and photosynthesis,” in Oxidative Damage to Plants: Antioxidant Networks and Signaling, ed. Ahmad P., (Elsevier Inc.), 1–63. 10.1016/B978-0-12-799963-0.00001-0
Hansen P. D., (2003). “Biomarkers,” in Bioindicators and Biomonitors, eds Markert B. A., Breure A. M., Zechmeiste H. G., (Elsevier Science Ltd.), 203–220. Available online at: https://www.sciencedirect.com/bookseries/trace-metals-and-other-contaminants-in-the-environment/vol/6
Hanson A. D., Rivoal J., Paquet L., Cage D. A., (1994). Biosynthesis of 3-dimethylsulfoniopropionate in Wollastonia biflora (L.) DC. Plant Physiol. 105, 103–110. 10.1104/pp.105.1.1038029347
Hardisky M. A., Klemas V., Smart R. M., (1983). The influence of soil salinity, growth form, and leaf moisture on the spectral radiance of Spartina alterniflora canopies. Photogramm. Eng. Remote Sens. 49, 77–83.
Hatton A. D., Wilson S. T., (2007). Particulate dimethylsulphoxide and dimethylsulphoniopropionate in phytoplankton cultures and Scottish coastal waters. Aquat. Sci. 69, 330–340. 10.1007/s00027-007-0891-4
Hedley J. D., McMahon K., Fearns P., (2014). Seagrass canopy photosynthetic response is a function of canopy density and light environment: a model for Amphibolis griffithii. PLoS ONE 9:e111454. 10.1371/journal.pone.011145425347849
Husband J., Kiene R., (2007). Occurrence of dimethylsulfoxide in leaves, stems, and roots of Spartina alterniflora. Wetlands 27, 224–229. 10.1672/0277-5212(2007)27[224:OODILS]2.0.CO;2
Husband J. D., (2007). The role of DMSP in oxidative stress protection in Spartina alterniflora Loisel (PhD thesis). University of South Alabama, Mobile, AL, United States.
Husband J. D., Kiene R. P., Sherman T. D., (2012). Oxidation of dimethylsulfoniopropionate (DMSP) in response to oxidative stress in Spartina alterniflora and protection of a non-DMSP producing grass by exogenous DMSP+acrylate. Environ. Exp. Bot. 79, 44–48. 10.1016/j.envexpbot.2012.01.006
Jackson G., Stuckey J., (2007). Effects of dimethylsulfoniopropionate (DMSP) produced by the cordgrass Spartina alterniflora on its epiphytic algal community. Aquat. Sci. 69, 419–426. 10.1007/s00027-007-0890-5
Jackson G., Zingmark R., Lewitus A. J., Tymowski R. G., Stuckey J., (2006). Spatial and temporal dynamics of epiphytic microalgae on the cordgrass Spartina alterniflora in North Inlet Estuary, South Carolina. Estuaries Coasts 29, 1212–1221. 10.1007/BF02781821
Jacquemart J., Demoulin V., (2006). Inventaire des macroalgues épiphytes des feuilles de Posidonia oceanica (L.) Delile dans la Baie de la Revellata (Calvi, Corse). Lejeunia Rev Bot 181:71. Available online at: https://popups.uliege.be:443/0457-4184/index.php?id=464
Kamenos N. A., Strong S. C., Shenoy D. M., Wilson S. T., Hatton A. D., Geoffrey Moore P., (2008). Red coralline algae as a source of marine biogenic dimethylsulphoniopropionate. Mar. Ecol. Prog. Ser. 372, 61–66. 10.3354/meps07687
Karsten U., Wiencke C., Kirst G. O., (1992). Dimethylsulphoniopropionate (DMSP) accumulation in green macroalgae from polar to temperate regions: interactive effects of light versus salinity and light versus temperature. Polar Biol. 12, 603–607. 10.1007/BF00236983
Kiene R. P., Gerard G., (1994). Determination of trace levels of dimethylsulfoxide (DMSO) in seawater and rainwater. Mar. Chem. 47, 1–12. 10.1016/0304-4203(94)90009-4
Lee P. A., de Mora S. J., (1999). Intracellular dimethylsulfoxide (DMSO) in unicellular marine algae: speculations on its origin and possible biological role. J. Phycol. 35, 8–18. 10.1046/j.1529-8817.1999.3510008.x
Lee P. A., De.Mora S. J., Levasseur M., (1999). A review of dimethylsulfoxide in aquatic environments. Atmos. Ocean 37, 439–456. 10.1080/07055900.1999.9649635
Lesser M. P., (2006). Oxidative stress in marine environments: biochemistry and physiological ecology. Annu. Rev. Physiol. 68, 253–278. 10.1146/annurev.physiol.68.040104.11000116460273
Lopez y Royo C., Casazza G., Pergent-Martini C., Pergent G., (2010). A biotic index using the seagrass Posidonia oceanica (BiPo), to evaluate ecological status of coastal waters. Ecol. Indic. 10, 380–389. 10.1016/j.ecolind.2009.07.005
Lopez y Royo C., Pergent G., Alcoverro T., Buia M. C., Casazza G., Martínez-Crego B., et al. (2011). The seagrass Posidonia oceanica as indicator of coastal water quality: experimental intercalibration of classification systems. Ecol. Indic. 11, 557–563. 10.1016/j.ecolind.2010.07.012
Lovelock E. J., Maggs R. J., (1972). Atmospheric dimethyl sulphide and the natural sulfur cycle. Nature 237, 452–453. 10.1038/237452a0
Luy N., Gobert S., Sartoretto S., Biondo R., Bouquegneau J. M., Richir J., (2012). Chemical contamination along the Mediterranean French coast using Posidonia oceanica (L.) Delile above-ground tissues: a multiple trace element study. Ecol. Indic. 18, 269–277. 10.1016/j.ecolind.2011.11.005
Lyons D. A., Scheibling R. E., Van Alstyne K. L., (2010). Spatial and temporal variation in DMSP content in the invasive seaweed Codium fragile ssp. fragile: effects of temperature, light and grazing. Mar. Ecol. Prog. Ser. 417, 51–61. 10.3354/meps08818
Martínez-Crego B., Arteaga P., Ueber A., Engelen A. H., Santos R., Molis M., (2015). Specificity in mesograzer-induced defences in seagrasses. PLoS ONE 10:e0141219. 10.1371/journal.pone.014121926506103
McCullagh P., Nedler J. A., (1989). Generalized Linear Models. London: Chapman and Hall/CRC. 10.1007/978-1-4899-3242-6
McDowell R. E., Amsler C. D., Dickinson D. A., McClintock J. B., Baker B. J., (2014a). Reactive oxygen species and the antarctic macroalgal wound response. J. Phycol. 50, 71–80. 10.1111/jpy.1212726988009
McDowell R. E., Amsler C. D., McClintock J. B., Baker B. J., (2014b). Reactive oxygen species as a marine grazing defense: H2O2 and wounded Ascoseira mirabilis both inhibit feeding by an amphipod grazer. J. Exp. Mar. Bio. Ecol. 458, 34–38. 10.1016/j.jembe.2014.04.012
McFarlin C. R., Alber M., (2013). Foliar DMSO:DMSP ratio and metal content as indicators of stress in Spartina alterniflora. Mar. Ecol. Prog. Ser. 474, 1–13. 10.3354/meps10184
Morris J. T., Sundareshwar P. V., Nietch C. T., Kjerfve B., Cahoon D. R., (2002). Responses of coastal wetlands to rising sea level. Ecology 83, 2869–2877. 10.1890/0012-9658(2002)083[2869:ROCWTR]2.0.CO;2
Mtwana Nordlund L., Koch E. W., Barbier E. B., Creed J. C., (2016). Seagrass ecosystem services and their variability across genera and geographical regions. PLoS ONE 11:e0163091. 10.1371/journal.pone.016309127732600
Muggeo V. M. R., (2003). Estimating regression models with unknown break-points. Stat. Med. 22, 3055–3071. 10.1002/sim.154512973787
Murchie E. H., Lawson T., (2013). Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J. Exp. Bot. 64, 3983–3998. 10.1093/jxb/ert20823913954
Nakajima K., (1989). Effects of High Concentrations of Dimethylthetin, Dimethyl-b-Propiothetin and Vitamin U on Young Rats. Takarazuka: Memoirs of Koshien University.
Norie J. W., (Ed.). (1831). “Section, V. I. The Islands of Corsica and Sardinia,” in New Piloting Directions for the Mediterranean Sea, the Adriatic, or Gulf of Venice, the Black Sea, Grecian Archipelago, and the Seas of Marmara and Azof (London: S. M'Dowall, Printer), 72–89.
Otte M. L., Morris J. T., (1994). Dimethylsulphoniopropionate (DMSP) in Spartina alterniflora Loisel. Aquat. Bot. 48, 239–259. 10.1016/0304-3770(94)90018-3
Otte M. L., Wilson G., Morris J. T., Moran B. M., (2004). Dimethylsulphoniopropionate (DMSP) and related compounds in higher plants. J. Exp. Bot. 55, 1919–1925. 10.1093/jxb/erh17815181109
Paquet L., Rathinasabapathi B., Saini H., Zamir L., Gage D., Huang Z. H., et al. (1994). Accumulation of the compatible solute 3-dimethylsulfoniopropionate in sugarcane and its relatives, but not other gramineous crops. Aust. J. Plant Physiol. 21, 37–48. 10.1071/PP9940037
Pearson R. K., (2001). Exploring process data. J. Process Control. 11, 179–194. 10.1016/S0959-1524(00)00046-9
Piazzi L., Balata D., Ceccherelli G., (2016). Epiphyte assemblages of the Mediterranean seagrass Posidonia oceanica: an overview. Mar. Ecol. 37, 3–41. 10.1111/maec.12331
Pinna S., Pais A., Chessa L., Nicola S., Ceccherelli G., (2009). Leaf partitioning of the seagrass Posidonia oceanica between two herbivores: is Sarpa salpa herbivory underestimated because of Paracentrotus lividus grazing? Estuar. Coast. Shelf Sci. 84, 21–27. 10.1016/j.ecss.2009.05.025
Pope S. B., Gadh R., (1988). Fitting noisy data using cross-validated cubic smoothing splines. Commun. Stat. Simul. Comput. 17, 349–376. 10.1080/03610918808812668
Prado P., Tomas F., Alcoverro T., Romero J., (2007). Extensive direct measurements of Posidonia oceanica defoliation confirm the importance of herbivory in temperate seagrass meadows. Mar. Ecol. Prog. Ser. 340, 63–71. 10.3354/meps340063
Quinn P. K., Bates T. S., (2011). The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 480, 51–56. 10.1038/nature1058022129724
Rhoades D. F., (1979). “Evolution of plant chemical defense against herbivores,” in Herbivores: Their Interactions With Secondary Plant Metabolites, eds Rosenthal G. A., Janzen D. H., (New York, NY: Academic Press), 3–54.
Richir J., Abadie A., Binard M., Biondo R., Borges A., Cimiterra N., et al. (2015). STARECAPMED (STAtion of Reference and rEsearch on change of local and global anthropogenic pressures on Mediterranean ecosystems drifts) - Année 2014. Calvi: Rapport de recherches, STARESO.
Rix L. N., Burdett H. L., Kamenos N. A., (2012). Irradiance-mediated dimethylsulphoniopropionate (DMSP) responses of red coralline algae. Estuar. Coast. Shelf Sci. 96, 268–272. 10.1016/j.ecss.2011.11.022
Roca G., Alcoverro T., Krause-Jensen D., Balsby T. J. S., van Katwijk M. M., Marbà N., et al. (2016). Response of seagrass indicators to shifts in environmental stressors: A global review and management synthesis. Ecol. Indic. 63, 310–323. 10.1016/j.ecolind.2015.12.007
Romero J., Martínez-Crego B., Alcoverro T., Pérez M., (2007). A multivariate index based on the seagrass Posidonia oceanica (POMI) to assess ecological status of coastal waters under the water framework directive (WFD). Mar. Pollut. Bull. 55, 196–204. 10.1016/j.marpolbul.2006.08.03217045301
RStudio Team. (2016). RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. Available online at: http://www.rstudio.com/.
Saha M., Rempt M., Gebser B., Grueneberg J., Pohnert G., Weinberger F., (2012). Dimethylsulphopropionate (DMSP) and proline from the surface of the brown alga Fucus vesiculosus inhibit bacterial attachment. Biofouling 28, 593–604. 10.1080/08927014.2012.69861522703021
Schober P., Boer C., Schwarte L. A., (2018). Correlation coefficients: Appropriate use and interpretation. Anesth. Analg. 126, 1763–1768. 10.1213/ANE.000000000000286429481436
Schultz J. C., Appel H. M., Ferrieri A. P., Arnold T. M., (2013). Flexible resource allocation during plant defense responses. Front. Plant Sci. 4:324. 10.3389/fpls.2013.0032423986767
Silva J., Sharon Y., Santos R., Beer S., (2009). Measuring seagrass photosynthesis: methods and applications. Aquat. Biol. 7, 127–141. 10.3354/ab00173
Simó R., Hatton A. D., Malin G., Liss P. S., (1998). Particulate dimethyl sulphoxide in seawater: production by microplankton. Mar. Ecol. Prog. Ser. 167, 291–296. 10.3354/meps167291
Simó R., Vila-Costa M., (2006). Ubiquity of algal dimethylsulfoxide in the surface ocean: geographic and temporal distribution patterns. Mar. Chem. 100, 136–146. 10.1016/j.marchem.2005.11.006
Slezak D., Herndl G. J., (2003). Effects of ultraviolet and visible radiation on the cellular concentrations of dimethylsulfoniopropionate (DMSP) in Emiliania huxleyi (strain L). Mar. Ecol. Prog. Ser. 246, 61–71. 10.3354/meps246061
Steele L., Darnell K. M., Cebrián J., Sanchez-Lizaso J. L., (2014). Sarpa salpa herbivory on shallow reaches of Posidonia oceanica beds. Anim. Biodivers. Conserv. 37, 49–57. Available online at: http://abc.museucienciesjournals.cat/volume-37-1-2014-abc/sarpa-salpa-herbivory-on-shallow-reaches-of-posidonia-oceanica-beds-2/?lang=en
Stefels J., (2000). Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J. Sea Res. 43, 183–197. 10.1016/S1385-1101(00)00030-7
Stefels J., Steinke M., Turner S., Malin G., Belviso S., (2007). “Environmental constraints on the production removal of the climatically active gas dimethylsulphide (DMS) implications for ecosystem modelling,” in Phaeocystis, Major Link in the Biogeochemical Cycling of Climate-Relevant Elements, eds van Leeuwe M. A., Stefels J., Belviso S., Lancelot C., Verity P. G., Gieskes W. W. C., (Dordrecht: Springer), 245–275. 10.1007/978-1-4020-6214-8_18
Sunda W., Kieber D. J., Kiene R. P., Huntsman S., (2002). An antioxydant function for DMSP and DMS in marine algae. Lett. Nat. 418, 317–320. 10.1038/nature0085112124622
Sundareshwar P. V., Morris J. T., Koepfler E. K., Fornwalt B., (2003). Phosphorus limitation of coastal ecosystem processes. Science 299, 563–565. 10.1126/science.107910012543975
Tomas F., Alvarez-Cascos D., Turon X., Romero J., (2006). Differential element assimilation by sea urchins Paracentrotus lividus in seagrass beds: implications for trophic interactions. Mar. Ecol. Prog. Ser. 306, 125–131. 10.3354/meps306125
Toms J. D., Lesperance M. L., (2003). Piecewise regression: a tool for identifying ecological thresolds. Ecology 84, 2034–2041. 10.1890/02-0472
Traer K., (1979). “The consumption of Posidonia oceanica Delile by Echinoids at the Isle of Ischia,” in Proceedings of the European Colloquium on Echinoderms, ed. Jangoux M., (Brussels).
Van Alstyne K. L., (2008). “Ecological and physiological roles of dimethylsulfoniopropionate and its products in marine macroalgae,” in Algal Chemical Ecology, ed. Amsler C. D., (Berlin; Heidelberg: Springer-Verlag), 173–194. 10.1007/978-3-540-74181-7_8
Van Alstyne K. L., Houser L. T., (2003). Dimethylsulfide release during macroinvertebrate grazing and its role as an activated chemical defense. Mar. Ecol. Prog. Ser. 250, 175–181. 10.3354/meps250175
Van Alstyne K. L., Puglisi M. P., (2007). DMSP in marine macroalgae and macroinvertebrates: distribution, function, and ecological impacts. Aquat. Sci. 69, 394–402. 10.1007/s00027-007-0888-z
Van Alstyne K. L., Wolfe G. V., Freidenburg T. L., Neill A., Hicken C. E., (2001). Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage. Mar. Ecol. Prog. Ser. 213, 53–65. 10.3354/meps213053
Van Diggelen J., Rozema J., Dickson D. M. J., Broekman R., (1986). Beta-3-dimethylsulphonioproprionate, proline and quaternary ammonium coumpounds in Spartina anglica in relation to sodium chloride, nitrogen and sulphur. New Phytol. 103, 573–586. 10.1111/j.1469-8137.1986.tb02894.x
Vassallo P., Paoli C., Rovere A., Montefalcone M., Morri C., Bianchi C. N., (2013). The value of the seagrass Posidonia oceanica: a natural capital assessment. Mar. Pollut. Bull. 75, 157–167. 10.1016/j.marpolbul.2013.07.04423953894
Vergés A., Becerro M. A., Alcoverro T., Romero J., (2007). Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica. Mar. Ecol. Prog. Ser. 343, 107–114. 10.3354/meps06885
Wittmann K., Mazzella L., Fresi E., (1981). Age specific patterns of leaf growth: their determination and importance for epiphytic colonization in Posidonia oceanica (L.) Delile. Rapp. Comm. Int. Mer. Mediter. 27, 189–192.
Wittmann K. J., (1984). Temporal and morphological variations of growth in a natural stand of Posidonia oceanica (L.) Delile. PSZNI Mar. Ecol. 5, 301–316. 10.1111/j.1439-0485.1984.tb00128.x
Wittmann K. J., Ott J. A., (1982). Effects of cropping on growth in the Mediterranean seagrass Posidonia oceanica (L.) Delile. PSZNI Mar. Ecol. 3, 151–159. 10.1111/j.1439-0485.1982.tb00380.x
Zhang L., Kuniyoshi I., Hirai M., Shoda M., (1991). Oxidation of dimethyl sulfide by Pseudomonas acidovorans DMR-11 isolated from peat biofilter. Biotechnol. Lett. 13, 223–228. 10.1007/BF01025822
Zheng Y., Bu N. S., Long X. E., Sun J., He C. Q., Liu X. Y., et al. (2017). Sulfate reducer and sulfur oxidizer respond differentially to the invasion of Spartina alterniflora in estuarine salt marsh of China. Ecol. Eng. 99, 182–190. 10.1016/j.ecoleng.2016.11.031
