Assessing the ecological status of seagrasses using morphology, biochemical descriptors and microbial community analyses. A study in Halophila stipulacea (Forsk.) Aschers meadows in the northern Red Sea

Ecological Indicators

Volumn 60, Issue , 2016, Pages 1150-1163

  Mejia, Astrid Y ^a   Rotini, Alice ^a   Lacasella, Federica ^b   Bookman, Revital ^c   Thaller, Maria Cristina ^a   Shem Tov, Rachamim ^d   Winters, Gidon ^d   Migliore, Luciana ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF HAIFA   (Israel)

^d The Dead Sea and Arava Science Center   (Israel)

Author keywords

Epiphytic microbial community; Halophila stipulacea; Photosynthetic pigments; Plant morphometrics; Seagrass monitoring; Total phenols

Indexed keywords

FORESTRY; HYDRODYNAMICS; INTEGRATED CONTROL; MICROORGANISMS; MORPHOLOGY; PHENOLS; PLANTS (BOTANY);

HALOPHILA STIPULACEA; MICROBIAL COMMUNITIES; MORPHOMETRICS; PHOTOSYNTHETIC PIGMENTS; SEAGRASSES; TOTAL PHENOLS;

ECOSYSTEMS;

BIOCHEMISTRY; ENVIRONMENTAL CHANGE; ENVIRONMENTAL CONDITIONS; HYDRODYNAMICS; INTEGRATED APPROACH; LIGHT AVAILABILITY; MEADOW; MICROBIAL COMMUNITY; MORPHOLOGY; SEAGRASS; SURFACE AREA;

ERITREA; GULF OF AQABA; INDIAN OCEAN; NORTHERN RED SEA; RED SEA [INDIAN OCEAN];

BACTEROIDETES; CYANOBACTERIA; GAMMAPROTEOBACTERIA; HALOPHILA STIPULACEA; RHODOBACTERACEAE;

EID: 84942785257     PISSN: 1470160X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecolind.2015.09.014     Document Type: Article

References (110)

1. A. Abelson, B. Shteinman, M. Fine, and S. Kaganovsky Mass transport from pollution sources to remote coral reefs in Eilat (Gulf of Aqaba, Red Sea) Mar. Pollut. Bull. 38 1 1999 25 29 10.1016/S0025-326X(99)80008-3
2. M.D. Abramoff, P.J. Magalhaes, and S.J. Ram Image processing with ImageJ Biophotonics Int. 11 7 2004 36 42
3. S. Agostini, J. Desjobert, and G. Pergent Distribution of phenolic compounds in the seagrass Posidonia oceanica Phytochemistry 48 1998 611 617
4. T.D. Ainsworth, R. Vega Thurber, and R.D. Gates The future of coral reefs: a microbial perspective Trends Ecol. Evol. 25 4 2010 233 240 10.1016/j.tree.2009.11.001
5. S. Al-Rousan, F. Al-Horani, E. Eid, and M. Khalaf Assessment of seagrass communities along the Jordanian coast of the Gulf of Aqaba, Red Sea Mar. Biol. Res. 7 2011 93 99 10.1080/17451001003660319
6. D.L. Angel, N. Eden, and L. Susel The influence of environmental variables on Halophila stipulacea growth H. Rosenthal, B. Moav, H. Gordin, Improving the Knowledge Base in Modern Aquaculture. European Aquaculture Society Special Publication No. 25 1995 103 128
7. L.V. Aragones, I.R. Lawler, W.J. Foley, and H. Marsh Dugong grazing and turtle cropping: grazing optimization in tropical seagrass systems? Oecologia 149 2006 635 647 10.1007/s00442-006-0477-1
8. T. Arnold, G. Freundlich, T. Weilnau, A. Verdi, and I.R. Tibbetts Impacts of groundwater discharge at Myora Springs (North Stradbroke Island, Australia) on the phenolic metabolism of eelgrass, Zostera muelleri, and grazing by the juvenile rabbitfish, Siganus fuscescens PLOS ONE 9 8 2014 e104738 10.1371/journal.pone.0104738
9. T. Arnold, C. Mealey, H. Leahey, A.W. Miller, J.M. Hall-Spencer, M. Milazzo, and K. Maers Ocean acidification and the loss of phenolic substances in marine plants PLoS ONE 7 4 2012 e35107 10.1371/journal.pone.0035107
10. T.M. Arnold, C.E. Tanner, M. Rothen, and J. Bullington Wound-induced accumulations of condensed tannins in turtlegrass, Thalassia testudinum Aquat. Bot. 89 2008 27 33 10.1016/j.aquabot.2008.02.001
11. ASTM Standard D6913 Standard Test Methods for Particle-Size Distribution (Gradation) of Soils Using Sieve Analysis 2009 10.1520/D6913-04R09E01 www.astm.org
12. C.E. Bagwell, J.R. La Rocque, G.W. Smith, S.W. Polson, M.J. Friez, J.W. Longshore, and C.R. Lovell Molecular diversity of diazotrophs in oligotrophic tropical seagrass bed communities FEMS Microbiol. Ecol. 39 2002 113 119 10.1111/j.1574-6941.2002.tb00912.x
13. S. Beer, M. Björk, and J. Beardal Photosynthesis in the Marine Environment, Part II 2014 John Wiley and Sons Ltd. Oxford, UK 61 66
14. R.N. Bennett, and R.M. Wallsgrove Secondary metabolites in plant defence mechanisms New Phytol. 127 1994 617 633 10.1111/j.1469-8137.1994.tb02968.x
15. M. Björk, F. Short, E. Mcleod, and S. Beer Managing Seagrasses for Resilience to Climate Change 2008 IUCN Gland, Switzerland
16. de W.F. Boer Seagrass-sediment interactions, positive feedbacks and critical thresholds for occurrence: a review Hydrobiologia 597 2007 5 24 10.1007/s10750-007-0780-9
17. M.C. Buia, M.C. Gambi, and M. Dappiano The seagrass ecosystems M.C. Gambi, M. Dappiano, Mediterranean Marine Benthos: A Manual for Its Sampling and Study Biol. Mar. Mediterr. 111 2004 133 183
18. S. Cabaço, R. Machás, and R. Santos Biomass-density relationship of the seagrass Zostera noltii: a tool for monitoring anthropogenic nutrient disturbance Estuar. Coast. Shelf Sci. 74 2007 557 564 10.1016/j.ecss.2007.05.029
19. S. Cabaço, R. Machás, and R. Santos Individual and population plasticity of the seagrass Zostera noltii along a vertical intertidal gradient Estuar. Coast. Shelf Sci. 82 2009 301 308 10.1016/j.ecss.2009.01.020
20. S. Campbell, C. Miller, A. Steven, and A. Stephens Photosynthetic responses of two temperate seagrasses across a water quality gradient using chlorophyll fluorescence J. Exp. Mar. Biol. Ecol. 291 2003 57 78 10.1016/S0022-0981(03)00090-X
21. L. Cariello, L. Zanetti, and S. De Stefano Posidonia ecosystem - V. Phenolic compounds from marine phanerogames, Cymodocea nodosa and Posidonia oceanica Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 62 2 1979 159 161
22. N.M. Cayabyab, and S. Enríquez Leaf photoacclimatory responses of the tropical seagrass Thalassia testudinum under mesocosm conditions: a mechanistic scaling-up study New Phytol. 176 1 2007 108 123 10.1111/j.1469-8137.2007.02147.x
23. K.R. Clarke, and R.M. Warwick Change in Marine Communities: An Approach to Statistical Analysis and Interpretation 2nd ed. 2001 PRIMER-E Plymouth 1 179
24. C.J. Collier, P.S. Lavery, P.J. Ralph, and R.J. Masini Shade-induced response and recovery of the seagrass Posidonia sinuosa J. Exp. Mar. Biol. Ecol. 370 2009 89 103 10.1016/j.jembe.2008.12.003
25. C.J. Collier, M. Waycott, and A.G. Ospina Responses of four Indo-West Pacific seagrass species to shading Mar. Pollut. Bull. 65 4 2012 342 354 10.1016/j.marpolbul.2011.06.017
26. R. Costanza, R. De Groot, P. Sutton, S. Van der Ploeg, S.J. Anderson, I. Kubiszewski, S. Farber, and R.K. Turner Changes in the global value of ecosystem services Glob. Environ. Change 26 2014 152 158 10.1016/j.gloenvcha.2014.04.002
27. J.M. Crawford, and J. Clardy Bacterial symbionts and natural products Chem. Commun. 47 2011 7559 7566 10.1039/c1cc11574j
28. B.C. Crump, and E.W. Koch Attached bacterial populations shared by four species of aquatic angiosperms Appl. Environ. Microbiol. 74 2008 5948 5957 10.1128/AEM.00952-08
29. H.Y. Dang, T.G. Li, M.N. Chen, and G.Q. Huang Cross-ocean distribution of Rhodobacterales bacteria as primary surface colonizers in temperate coastal marine waters Appl. Environ. Microbiol. 74 2008 52 60 10.1128/AEM.01400-07
30. K.M. Darnell, and K.L. Heck Jr. Species-specific effects of prior grazing on the palatability of turtle grass J. Exp. Mar. Biol. Ecol. 440 2013 225 232 10.1016/j.jembe.2012.12.012
31. R. Devereux Seagrass rhizosphere microbial communities E. Kristensen, R.R. Haese, J.E. Kostka, Interactions Between Macro- and Microorganisms in Marine Sediments. Coastal and Estuarine Studies 2005 American Geophysical Union Washington, DC 199 216
32. S.E. Dowd, Y. Sun, P.R. Secor, D.D. Rhoads, B.M. Wolcott, G.A. James, and R.D. Wolcott Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing BMC Microbiol. 8 2008 43 10.1186/1471-2180-8-43
33. C.M. Duarte Allometric scaling of seagrass form and productivity Mar. Ecol. Prog. Ser. 77 1991 289 300
34. C.M. Duarte, M. Holmer, and N. Marba Plant-microbe interactions in seagrass meadows E. Kristensen, R. Haese, J. Kotska, Macro- and Microorganisms in Marine Sediments. Coastal and Estuarine Studies 2005 American Geophysical Union Washington, DC 31 60
35. N. Dubilier, C. Bergin, and C. Lott Symbiotic diversity in marine animals: the art of harnessing chemosynthesis Nat. Rev. Microbiol. 6 2008 725 740 10.1038/nrmicro1992
36. S. Egan, T. Harder, C. Burke, P. Steinberg, S. Kjelleberg, and T. Thomas The seaweed holobiont: understanding seaweed-bacteria interaction FEMS Microbiol. Rev. 37 2012 462 476 10.1111/1574-6976.12011
37. A. El Shaffai A. Rouphael, A. Abdulla, A Field Guide to Seagrasses of the Red Sea 1st ed. 2011 IUCN/France Total Foundation Gland, Switzerland/Courbevoie 1 56
38. H. Elifantz, G. Horn, M. Ayon, Y. Cohen, and D. Minz Rhodobacteraceae are the key members of the microbial community of the initial biofilm formed in Eastern Mediterranean coastal seawater FEMS Microbiol. Ecol. 85 2 2013 348 357 10.1111/1574-6941.12122
39. S. Enriquez, N. Marbà, J. Cebriàn, and C.M. Duarte Annual variation in leaf photosynthesis and leaf nutrient content of four Mediterranean seagrasses Bot. Mar. 47 4 2004 295 306 10.1515/BOT.2004.035
40. L. Fan, D. Reynolds, M. Liu, M. Stark, S. Kjelleberg, N.S. Webster, and T. Thomas Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts PNAS 109 2012 E1878 E1887 10.1073/pnas.1203287109
41. L. Ferrat, C. Pergent-Martini, M. Romeo, and G. Pergent Hydrosoluble phenolic compounds production in a Mediterranean seagrass according to mercury contamination (Abstract) Gulf Mex. Sci. 21 1 2003 108
42. J.W. Fourqurean, C.M. Duarte, H. Kennedy, N. Marba, M. Holmer, M.A. Mateo, E.T. Apostolaki, G.A. Kendrick, D. Krause-Jensen, K.J. McGlathery, and O. Serrano Seagrass ecosystems as a globally significant carbon stock Nat. Geosci. 5 2012 505 509 10.1038/ngeo1477
43. J.A. Fuerst Beyond prokaryotes and eukaryotes: planctomycetes and cell organization Nat. Educ. 3 9 2010 44 online at: http://www.nature.com/scitable/topicpage/beyond-prokaryotes-and-eukaryotes-planctomycetes-and-cell-14158971
44. P. García-Marín, S. Cabaço, I. Hernández, J.J. Vergara, J. Silva, and R. Santos Multi-metric index based on the seagrass Zostera noltii (ZoNI) for ecological quality assessment of coastal and estuarine systems in SW Iberian Peninsula Mar. Pollut. Bull. 68 2013 46 54 10.1016/j.marpolbul.2012.12.025
45. M. García-Martínez, A. López-López, M.L. Calleja, N. Marbà, and C.M. Duarte Bacterial community dynamics in a seagrass (Posidonia oceanica) meadow sediment Estuar. Coasts 32 2009 276 286 10.1007/s12237-008-9115-y
46. K. Grasshoff, K. Kremling, and M. Ehrhardt Methods of Seawater Analysis 1999 Verlag Chemie Weinheim, Germany
47. E.P. Green, and F.T. Short World Atlas of Seagrasses 2003 University of California Press Berkeley
48. M.I. Hamisi, T.J. Lyimo, M. Muruke, and B. Bergman Nitrogen fixation by epiphytic and epibenthic diazotrophs associated with seagrass meadows along Tanzanian coast, Western Indian Ocean Aquat. Microb. Ecol. 57 2009 33 42 10.3354/ame01323
49. O. Hammer, and P.D. Ryan PAST - PAlaeontological STatistics, ver. 1.89, User's Manual 2009
50. 2-rich vent Environ. Microbiol. Rep. 7 3 2015 516 525 10.1111/1758-2229.12282
51. U. Hentschel, J. Piel, S.M. Degnan, and M.W. Taylor Genomic insights into the marine sponge microbiome Nat. Rev. Microbiol. 10 2012 641 654 10.1038/nrmicro2839
52. S.I. Jensen, M. Kul, and A. Priemé Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina FEMS Microbiol. Ecol. 62 2007 108 117 10.1111/j.1574-6941.2007.00373.x
53. 2 gradient in the Mediterranean sea off Vulcano, Italy Microb. Ecol. 67 4 2014 819 828 10.1007/s00248-014-0368-7
54. H. Kadivar, and A.E. Stapleton Ultraviolet radiation alters maize phyllosphere bacterial diversity Microb. Ecol. 45 2003 353 361 10.1007/s00248-002-1065-5
55. K. Küsel, H.C. Pinkart, H.L. Drake, and R. Devereux Acetogenic and sulfate-reducing bacteria inhabiting the rhizoplane and deep cortex cells of the sea grass Halodule wrightii Appl. Environ. Microbiol. 65 11 1999 5117 5123
56. H.K. Lichtenthaler, and F. Babani Light adaption and senescence of the photosynthetic apparatus. Changes in pigment composition, Chlorophyll fluorescence parameters and photosynthetic activity G.C. Papageorgiou, Govindjee Chlorophyll Fluorescence: A Signature of Photosynthesis 2004 Springer Dordrecht 713 736
57. B.J. Longstaff, N.R. Loneragan, M.J. O'Donohue, and W.C. Dennison Effects of light deprivation on the survival and recovery of the seagrass Halophila ovalis (R.Br.) Hook J. Exp. Mar. Biol. Ecol. 234 1999 1 27 10.1016/S0022-0981(98)00137-3
58. Y. Loya, H. Lubinevsky, M. Rosenfeld, and E. Kramarsky-Winter Nutrient enrichment caused by in situ fish farms at Eilat, Red Sea is detrimental to coral reproduction Mar. Pollut. Bull. 49 2004 344 353 10.1016/j.marpolbul.2004.06.011
59. C. Lozupone, M.E. Lladser, D. Knights, J. Stombaugh, and R. Knight UniFrac: an effective distance metric for microbial community comparison ISME J. 5 2011 169 172 10.1038/ismej.2010.133
60. N. Marbà, D. Krause-Jensen, T. Alcoverro, S. Birk, A. Pedersen, J.M. Neto, S. Orfanidis, J.M. Garmendia, I. Muxika, A. Borja, K. Dencheva, and C.M. Duarte Diversity of European seagrass indicators: patterns within and across regions Hydrobiologia 704 2013 265 278 10.1007/s10750-012-1403-7
61. E.M. Marzinelli, A.H. Campbell, E. Zozaya Valdes, A. Vergés, S. Nielsen, T. Wernberg, T. de Bettignies, S. Bennett, J.G. Caporaso, T. Thomas, and P.D. Steinberg Continental-scale variation in seaweed host-associated bacterial communities is a function of host condition, not geography Environ. Microbiol. 2015 10.1111/1462-2920.12972 (pre-press, online from 04.08.15)
62. L.J. McKenzie, W.J. Lee Long, R.G. Coles, and C.A. Roder Seagrass-Watch: community based monitoring of seagrass resources Biol. Mar. Mediterr. 7 2 2000 393 396
63. D. Meron, E. Atias, L.I. Kruh, H. Elifantz, D. Minz, M. Fine, and E. Banin The impact of reduced pH on the microbial community of the coral Acropora eurystoma ISME J. 5 2011 51 60 10.1038/ismej.2010.102
64. L. Migliore, A. Rotini, D. Randazzo, N.N. Albanese, and A. Giallongo Phenols content and 2-D electrophoresis protein pattern: a promising tool to monitor Posidonia meadows health state BMC Ecol. 7 2007 6 10.1186/1472-6785-7-6
65. L. Migliore, A. Piccenna, A. Rotini, S. Garrard, and M.C. Buia Can ocean acidification affect chemical defenses in Posidonia oceanica? Proc. Med. Seagrass Work Essaouira, Morocco 2012 14
66. NMP Israel's National Monitoring of the Gulf of Eilat 2014 http://www.meteo-tech.co.il/EilatYam-data/ey-data.asp
67. R. Orth, T. Carruthers, W. Dennison, C. Duarte, J. Fourqurean, K. Heck, A. Hughes, G. Kendrick, W. Kenworthy, S. Olyarnik, F. Short, M. Waycott, and S. Williams A global crisis for seagrass ecosystems BioScience 56 2006 987 996
68. G. Peralta, F.G. Brun, I. Hernández, J.J. Vergara, and J.L. Pérez-Lloréns Morphometric variations as acclimation mechanisms in Zostera noltii beds Estuar. Coast. Shelf Sci. 64 2005 347 356 10.1016/j.ecss.2005.02.027
69. G. Peralta, F.G. Brun, J.L. Pérez-Lloréns, and T.J. Bouma Direct effects of current velocity on the growth, morphometry and architecture of seagrasses: a case study on Zostera noltii Mar. Ecol. Prog. Ser. 327 2006 135 142
70. G. Pergent, C.F. Boudouresque, O. Dumay, C. Pergent- Martini, and S. Wyllie-Echeverria Competition between the invasive macrophyte Caulerpa taxifolia and the seagrass Posidonia oceanica: contrasting strategies BMC Ecol. 8 2008 20 10.1186/1472-6785-8-20
71. R. Quakenbush, D. Bunn, and W. Lingren HPLC determination of phenolic acids in the watersoluble extract of Zostera marina L. (eelgrass) Aquat. Bot. 24 1986 83 89 10.1016/0304-3770(86)90119-1
72. P.J. Ralph, M.J. Durako, S. Enríquez, C.J. Collier, and M.A. Doblin Impact of light limitation on seagrasses J. Exp. Mar. Biol. Ecol. 350 2007 176 193 10.1016/j.jembe.2007.06.017
73. J. Romero, B. Martínez-Crego, T. Alcoverro, and A. Pérez 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 2007 196 204 10.1016/j.marpolbul.2006.08.032
74. E. Rosenberg, O. Koren, L. Reshef, R. Efrony, and I. Zilber-Rosenberg The role of microorganisms in coral health, disease and evolution Nat. Rev. Microbiol. 5 2007 355 362 10.1038/nrmicro1635
75. A. Rotini, A. Belmonte, I. Barrote, C. Micheli, A. Peirano, R. Santos, J. Silva, and L. Migliore Effectiveness and consistency of a suite of descriptors to assess the ecological status of seagrass meadows (Posidonia oceanica L. Delile) Estuar. Coast. Shelf Sci. 130 2013 252 259 10.1016/j.ecss.2013.06.015
76. A. Rotini, L. Anello, M. Di Bernardo, A. Giallongo, L. Valiante, and L. Migliore Comparative analysis of bed density, total phenol content and protein expression pattern in Posidonia oceanica (L.) Delile Open J. Ecol. 3 2013 438 444 10.4236/oje.2013.36050
77. A. Rotini, C. Micheli, L. Valiante, and L. Migliore Assessment of Posidonia oceanica (L.) Delile conservation status by standard and putative approaches: the case study of Santa Marinella meadow (Italy, W Mediterranean) Open J. Ecol. 1 2011 48 56 10.4236/oje.2014.46027
78. P.D. Schloss, S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, R.A. Lesniewski, B.B. Oakley, D.H. Parks, C.J. Robinson, J.W. Sahl, B. Stres, G.G. Thallinger, D.J. Van Horn, and C.F. Weber Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities Appl. Environ. Microb. 75 23 2009 7537 7541 10.1128/AEM.01541-09
79. A. Schmalenberger, F. Schwieger, and C.C. Tebbe Effect of primers hybridizing to different evolutionarily conserved regions of the small-subunit rRNA gene in PCR-based microbial community analyses and genetic profiling Appl. Environ. Microbiol. 67 2000 3557 3563 10.1128/AEM.67.8.3557-3563.2001
80. F. Schwieger, and C.C. Tebbe A new approach to utilize PCR-single-strand-conformation polymorphism for 16S rRNA gene-based microbial community analysis Appl. Environ. Microbiol. 64 1998 4870 4876
81. Y. Sharon, and S. Beer Diurnal movements of chloroplasts in Halophila stipulacea and their effect on PAM fluorometric measurements of photosynthetic rates Aquat. Bot. 88 4 2008 273 276 10.1016/j.aquabot.2007.11.006
82. Y. Sharon, J. Silva, R. Santos, J.W. Runcie, M. Chernihovsky, and S. Beer Photosynthetic responses of Halophila stipulacea to a light gradient. II. Acclimations following transplantation Aquat. Biol. 7 1/2 2009 153 157 10.3354/ab00148
83. Y. Sharon, O. Levitan, D. Spungin, I. Berman-Frank, and S. Beer Photoacclimation of the seagrass Halophila stipulacea to the dim irradiance at its 48-meter depth limit Limnol. Oceanogr. 56 2011 357 362 10.4319/lo.2011.56.1.0357
84. F.T. Short, L.J. McKenzie, R.G. Coles, and J.L. Gaeckle SeagrassNet Manual for Scientific Monitoring of Seagrass Habitat Western Pacific edition 2004 Queensland Department of Primary Industries Cairns, Australia 1 71 http://www.SeagrassNet.org
85. F.T. Short, L.J. McKenzie, R.G. Coles, and J.L. Gaeckle SeagrassNet Manual for Scientific Monitoring of Seagrass Habitat Caribbean edition 2005 University of New Hampshire Durham, NH, USA 1 74 http://www.SeagrassNet.org
86. F.T. Short, B. Polidoro, S.R. Livingstone, K.E. Carpenter, S. Bandeira, J.S. Bujang, H.P. Calumpong, T.J.B. Carruthers, R.G. Coles, and et al. Extinction risk assessment of the world's seagrass species Biol. Conserv. 144 2011 1961 1971 10.1016/j.biocon.2011.04.010
87. N. Schubert, M.F. Colombo-Pallota, and S. Enríquez Leaf and canopy scale characterization of the photoprotective response to high-light stress of the seagrass Thalassia testudinum Limnol. Oceanogr. 60 1 2015 286 302 10.1002/lno.10024
88. R.D. Sieg, and J. Kubanek Chemical ecology of marine angiosperms: opportunities at the interface of marine and terrestrial systems J. Chem. Ecol. 39 2013 687 711 10.1007/s10886-013-0297-9
89. J. Silva, I. Barrote, M. Costa, S. Albano, and R. Santos Physiological responses of Zostera marina and Cymodocea nodosa to light-limitation stress PLOS ONE 8 11 2013 e81058 10.1371/journal.pone.0081058
90. J. Silverman, B. Lazar, and J. Erez Community metabolism of a coral reef exposed to naturally varying dissolved inorganic nutrient loads Biogeochemistry 84 1 2007 67 82 10.1007/s10533-007-9075-5
91. R.P. Singh, and C.R.K. Reddy Seaweed-microbial interactions: key functions of seaweed-associated bacteria FEMS Microbiol. Ecol. 88 2014 213 230 10.1111/1574-6941.12297
92. L.J. Stal, H. van Gemerden, and W.E. Krumbein Structure and development of a benthic marine microbial mat FEMS Microbiol. Ecol. 31 2 1985 111 125 10.1016/0378-1097(85)90007-2
93. L. Steele, M. Caldwell, A. Boettcher, and T. Arnold Seagrass-pathogen interactions: 'pseudo-induction' of turtlegrass phenolics near wasting disease lesions Mar. Ecol. Prog. Ser. 303 2005 123 131 10.3354/meps303123
94. L. Steele, and J.F. Valentine Idiosyncratic responses of seagrass phenolic production following sea urchin grazing Mar. Ecol. Prog. Ser. 466 2012 81 92 10.3354/meps09921
95. E. Teira, S. Martínez-García, A. Calvo-Díaz, and X.A.G. Morán Effects of inorganic and organic nutrient inputs on bacterioplankton community composition along a latitudinal transect in the Atlantic Ocean Aquat. Microb. Ecol. 60 2010 299 313 10.3354/ame01435
96. R.K.F. Unsworth, M. van Keulen, and R.G. Coles Seagrass meadows in a globally changing environment Mar. Pollut. Bull. 83 2 2014 383 386 10.1016/j.marpolbul.2014.02.026
97. L.H.T. Vergeer, T.L. Aarts, and J.D. De Groot The 'wasting disease' and the effect of abiotic factors (light intensity, temperature, salinity) and infection with Labyrinthula zosterae on the phenolic content of Zostera marina shoots Aquat. Bot. 52 1 1995 35 44
98. L.H.T. Vergeer, and A. Develi Phenolic acids in healthy and infected leaves of Zostera marina and their growth-limiting properties towards Labyrinthula zosterae Aquat. Bot. 58 1997 65 72 10.1016/S0304-3770(96)01115-1
99. A. Vergés, M.A. Becerro, T. Alcoverro, and J. Romero Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica Mar. Ecol. Prog. Ser. 343 2007 107 114
100. A. Vergés, M. Perez, T. Alcoverro, and J. Romero Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish Oecologia 155 2008 751 760 10.1007/s00442-007-0943-4
101. M. Wahl, F. Goecke, A. Labes, S. Dobretsov, and F. Weinberger The second skin: ecological role of epibiotic biofilms on marine organisms Front. Microbiol. 3 2012 292 10.3389/fmicb.2012.00292
102. M. Waycott, C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean, K.L. Heck, A.R. Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short, and S.L. Williams Accelerating loss of seagrasses across the globe threatens coastal ecosystems Proc. Natl. Acad. Sci. U. S. A. 106 2009 12377 12381 10.1073/pnas.0905620106
103. N.S. Webster, R.E. Cobb, and A.P. Negri Temperature thresholds for bacterial symbiosis with a sponge ISME J. 2 2008 830 842 10.1038/ismej.2008.42
104. N.S. Webster, and D.G. Bourne Microbes E.S. Poloczanska, A.J. Hobday, A.J. Richardson, Marine Climate Change Impacts and Adaptation Report Card for Australia 2012 2012 1 17 http://www.oceanclimatechange.org.au
105. S. Weidner, W. Arnold, E. Stackebrandt, and A. Puhler Phylogenetic analysis of bacterial communities associated with leaves of the seagrass Halophila stipulacea by a culture-independent small-subunit rRNA gene approach Appl. Environ. Microbiol. 39 2000 22 31 10.1007/s002489900194
106. A.R. Wellburn The spectral determination of chlorophylls A and B, as well as total carotenoids, using various solvents with spectrophotometers of different resolution J. Plant Physiol. 144 1994 307 313
107. C.K. Wentworth A scale of grade and class terms for clastic sediments J. Geol. 30 5 1922 377 392
108. V. Witt, C. Wild, K.R.N. Anthony, G. Diaz-Pulido, and S. Uthicke Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef Environ. Microbiol. 13 11 2011 2976 2989 10.1111/j.1462-2920.2011.02571.x
109. V. Witt, C. Wild, and S. Uthicke Terrestrial runoff controls the bacterial community composition of biofilms along a water quality gradient in the Great Barrier Reef Appl. Environ. Microbiol. 78 21 2012 7786 7791 10.1128/AEM.01623-12
110. O. Zapata, and C. McMillan Phenolic acids in seagrasses Aquat. Bot. 7 1979 307 331