Epiphyte dynamics and carbon metabolism in a nutrient enriched Mediterranean seagrass (Posidonia oceanica) ecosystem

Journal of Sea Research

Volumn 66, Issue 2, 2011, Pages 135-142

  Apostolaki, Eugenia T ^a,b   Holmer, Marianne ^c   Marbà, Núria ^d   Karakassis, Ioannis ^a  

^a INSTITUTE OF OCEANOGRAPHY   (Greece)

^b UNIVERSITY OF CRETE   (Greece)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

Author keywords

Community Production; Dissolved Organic Carbon; Eutrophication; Herbivory; Metabolism; Nutrient Cycling

Indexed keywords

ABOVEGROUND BIOMASS; AQUACULTURE EFFLUENT; BIOLOGICAL PRODUCTION; BOTTOM-UP CONTROL; CAGE CULTURE; DISSOLVED ORGANIC CARBON; EPIPHYTE; EUTROPHICATION; FISH; HERBIVORY; MARINE ECOSYSTEM; METABOLISM; PLANT-HERBIVORE INTERACTION; SEAGRASS; SUBSTRATE; TEMPORAL VARIATION; TOP-DOWN CONTROL;

AEGEAN SEA; GREECE; MEDITERRANEAN SEA;

POSIDONIA OCEANICA;

EID: 80051696048     PISSN: 13851101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.seares.2011.05.007     Document Type: Article

References (68)

1. Alcoverro T., Manzanera M., Romero J. Nutrient mass balance of the seagrass Posidonia oceanica: the importance of nutrient translocation. Mar. Ecol. Prog. Ser. 2000, 194:13-21.
2. Apostolaki E.T., Holmer M., Marba N., Karakassis I. Degrading seagrass (Posidonia oceanica) ecosystems: a source of dissolved matter to the Mediterranean. Hydrobiologia 2010, 649:13-23.
3. Apostolaki E.T., Holmer M., Marba N., Karakassis I. Metabolic imbalance in coastal vegetated (Posidonia oceanica) and unvegetated benthic ecosystems. Ecosystems 2010, 13:459-471.
4. Apostolaki, E.T., Holmer, M., Marba, N., Karakassis, I., submitted for publication-a. Sediment nutrient enrichment reduces carbon sequestration in a Mediterranean seagrass (Posidonia oceanica) ecosystem.
5. Apostolaki E.T., Marba N., Holmer M., Karakassis I. Fish farming enhances biomass and nutrient loss in Posidonia oceanica (L.) Delile. Estuar. Coast. Shelf Sci. 2009, 81:390-400.
6. Apostolaki E.T., Marba N., Holmer M., Karakassis I. Fish farming impact on decomposition of Posidonia oceanica litter. J. Exp. Mar. Biol. Ecol. 2009, 369:58-64.
7. Apostolaki E.T., Tsagaraki T., Tsapakis M., Karakassis I. Fish farming impact on sediments and macrofauna associated with seagrass meadows in the Mediterranean. Estuar. Coast. Shelf Sci. 2007, 75:408-416.
8. Apostolaki, E.T., Vizzini, S., Karakassis, I., submitted for publication-b. Leaf vs. epiphyte nitrogen uptake in a Mediterranean seagrass (Posidonia oceanica) meadow under organic enrichment. Aquat. Bot.
9. Balata D., Piazzi L., Nesti U., Bulleri F., Bertocci I. Effects of enhanced loads of nutrients on epiphytes on leaves and rhizomes of Posidonia oceanica. J. Sea Res. 2010, 63:173-179.
10. Barron C., Duarte C.M. Dissolved organic matter release in a Posidonia oceanica meadow. Mar. Ecol. Prog. Ser. 2009, 374:75-84.
11. Barron, C., Duarte, C.M., in preparation. Dissolved organic matter release by marine macrophytes.
12. Barron C., Duarte C.M., Frankignoulle M., Borges A.V. Organic carbon metabolism and carbonate dynamics in a Mediterranean seagrass (Posidonia oceanica) meadow. Estuaries Coasts 2006, 29:417-426.
13. Ben Brahim M., Hamza A., Hannachi I., Rebai A., Jarboui O., Bouain A., Aleya L. Variability in the structure of epiphytic assemblages of Posidonia oceanica in relation to human interferences in the Gulf of Gabes, Tunisia. Mar. Environ. Res. 2010, 70:411-421.
14. Borowitzka M.A., Lavery P.S., van Keulen M. Epiphytes of seagrasses. Seagrasses: Biology, Ecology and Conservation 2006, 441-461. Springer, The Netherlands. A.W.D. Larkum, R.J. Orth, C.M. Duarte (Eds.).
15. Burton J.D., Riley J.P. Determination of soluble phosphate, and total phosphorus in sea-water and of total phosphorus in marine muds. Mikrochim. Acta 1956, 9:1350-1365.
16. Cebrian J., Enriquez S., Fortes M., Agawin N.S.R., Vermaat J., Duarte C.M. Epiphyte accrual on Posidonia oceanica (L.) Delile leaves: implications for light absorption. Bot. Mar. 1999, 42:123-128.
17. Cornelisen C.D., Thomas F.I.M. Ammonium and nitrate uptake by leaves of the seagrass Thalassia testudinum: impact of hydrodynamic regime and epiphyte cover on uptake rates. J. Mar. Syst. 2004, 49:177-194.
18. Dalsgaard T., Krause-Jensen D. Monitoring nutrient release from fish farms with macroalgal and phytoplankton bioassays. Aquaculture 2006, 256:302-310.
19. Diaz-Almela E., Marba N., Alvarez E., Santiago R., Holmer M., Grau A., Danovaro R., Argyrou M., Karakassis I., Duarte C.M. Benthic input rates predict seagrass (Posidonia oceanica) fish farm-induced decline. Mar. Pollut. Bull. 2008, 56:1332-1342.
20. Ferdie M., Fourqurean J.W. Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnol. Oceanogr. 2004, 49:2082-2094.
21. Fourqurean J.W., Muth M.F., Boyer J.N. Epiphyte loads on seagrasses and microphytobenthos abundance are not reliable indicators of nutrient availability in oligotrophic coastal ecosystems. Mar. Pollut. Bull. 2010, 60:971-983.
22. Frankovich T.A., Fourqurean J.W. Seagrass epiphyte loads along a nutrient availability gradient, Florida Bay, USA. Mar. Ecol. Prog. Ser. 1997, 159:37-50.
23. Frederiksen M., 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. Mar. Ecol. Prog. Ser. 2007, 345:93-104.
24. Gacia E., Costalago D., Prado P., Piorno D., Tomas F. Mesograzers in Posidonia oceanica meadows: an update of data on gastropod-epiphyte-seagrass interactions. Bot. Mar. 2009, 52:439-447.
25. Giovannetti E., Lasagna R., Montefalcone M., Bianchi C.N., Albertelli G., Morri C. Inconsistent responses to substratum nature in Posidonia oceanica meadows: an integration through complexity levels?. Chem. Ecol. 2008, 24:83-91.
26. Giovannetti E., Montefalcone M., Morri C., Bianchi C.N., Albertelli G. Early warning response of Posidonia oceanica epiphyte community to environmental alterations (Ligurian Sea, NW Mediterranean). Mar. Pollut. Bull. 2010, 60:1031-1039.
27. Heck K.L., Valentine J.F. Plant-herbivore interactions in seagrass meadows. J. Exp. Mar. Biol. Ecol. 2006, 330:420-436.
28. Hedges J.I., Stern J.H. Carbon and nitrogen determinations of carbonate-containing solids. Limnol. Oceanogr. 1984, 29:657-663.
29. Heijs S.K., Azzoni R., Giordani G., Jonkers H.M., Nizzoli D., Viaroli P., van Gemerden H. Sulfide-induced release of phosphate from sediments of coastal lagoons and the possible relation to the disappearance of Ruppia sp. Aquat. Microb. Ecol. 2000, 23:85-95.
30. Holmer M., Argyrou M., Dalsgaard T., Danovaro R., Diaz-Almela E., Duarte C.M., Frederiksen M., Grau A., Karakassis I., Marba N., Mirto S., Perez M., Pusceddu A., Tsapakis M. Effects of fish farm waste on Posidonia oceanica meadows: synthesis and provision of monitoring and management tools. Mar. Pollut. Bull. 2008, 56:1618-1629.
31. Holmer M., Duarte C.M., Boschker H.T.S., Barron C. Carbon cycling and bacterial carbon sources in pristine and impacted Mediterranean seagrass sediments. Aquat. Microb. Ecol. 2004, 36:227-237.
32. Holmer M., Frederiksen M. Stimulation of sulfate reduction rates in Mediterranean fish farm sediments inhabited by the seagrass Posidonia oceanica. Biogeochemistry 2007, 85:169-184.
33. Holmer M., Marba N., Diaz-Almela E., Duarte C.M., Tsapakis M., Danovaro R. Sedimentation of organic matter from fish farms in oligotrophic Mediterranean assessed through bulk and stable isotope (δ13C and δ15N) analyses. Aquaculture 2007, 262:268-280.
34. Holmer M., Perez M., Duarte C.M. Benthic primary producers - a neglected environmental problem in Mediterranean maricultures?. Mar. Pollut. Bull. 2003, 46:1372-1376.
35. Ivancic I., Deggobis D. An optimal manual procedure for ammonia analysis in natural waters by the indophenol blue method. Water Res. 1984, 18:1143-1147.
36. Karakassis I., Pitta P., Krom M.D. Contribution of fish farming to the nutrient loading of the Mediterranean. Sci. Mar. 2005, 62:313-321.
37. Karakassis I., Tsapakis M., Hatziyanni E. Seasonal variability in sediment profiles beneath fish farm cages in the Mediterranean. Mar. Ecol. Prog. Ser. 1998, 162:243-252.
38. Kruzic P. Variations in Posidonia oceanica meadow structure along the coast of the Dugi Otok Island (eastern Adriatic Sea). J. Mar. Biol. Assoc. U. K. 2008, 88:883-892.
39. Leoni V., Pasqualini V., Pergent-Martini C., Vela A., Pergent G. Physiological responses of Posidonia oceanica to experimental nutrient enrichment of the canopy water. J. Exp. Mar. Biol. Ecol. 2007, 349:73-83.
40. Lepoint G., Jacquemart J., Bouquegneau J.M., Demoulin V., Gobert S. Field measurements of inorganic nitrogen uptake by epiflora components of the seagrass Posidonia oceanica (Monocotyledons, Posidoniaceae). J. Phycol. 2007, 43:208-218.
41. Lin H.-J., Nixon S.W., Taylor D.I., Granger S.L., Buckley B.A. Responses of epiphytes on eelgrass, Zostera marina L., to separate and combined nitrogen and phosphorus enrichment. Aquat. Bot. 1996, 52:243-258.
42. Marba N., Santiago R., Diaz-Almela E., Alvarez E., Duarte C.M. Seagrass (Posidonia oceanica) vertical growth as an early indicator of fish-farm-derived stress. Estuar. Coast. Shelf Sci. 2006, 67:475-483.
43. McRoy C.P., Goering J.J. Nutrient transfer between the seagrass Zostera marina and its epiphytes. Nature 1974, 248:173-174.
44. Moore K.A., Wetzel R.L. Seasonal variations in eelgrass (Zostera marina L.) responses to nutrient enrichment and reduced light availability in experimental ecosystems. J. Exp. Mar. Biol. Ecol. 2000, 244:1-28.
45. Ouisse V., Migne A., Davoult D. Seasonal variations of community production, respiration and biomass of different primary producers in an intertidal Zostera noltii bed (Western English Channel, France). Hydrobiologia 2010, 649:3-11.
46. Oviatt C.A., Rudnick D.T., Keller A.A., Sampou P.A., Almquist G.T. A comparison of system (O2 and CO2) and C-14 measurements of metabolism in estuarine mesocosms. Mar. Ecol. Prog. Ser. 1986, 28:57-67.
47. Peirano A., Cocito S., Banfi V., Cupido R., Damasso V., Farina G., Lombardi C., Mauro R., Morri C., Roncarolo I., Saldana S., Savini D., Sgorbini S., Silvestri C., Stoppelli N., Torricelli L., Bianchi C.N. Phenology of the Mediterranean seagrass Posidonia oceanica (L.) Delile: medium and long-term cycles and climate inferences. Estuar. Coast. Shelf Sci. 2011, 94:77-92.
48. Peirano A., Niccolai I., Mauro R., Bianchi C.N. Seasonal grazing and food preference of herbivores in a Posidonia oceanica meadow. Sci. Mar. 2001, 65:367-374.
49. Penhale P.A., Smith W.O.J. Excretion of dissolved organic carbon by eelgrass (Zostera marina) and its epiphytes. Limnol. Oceanogr. 1977, 22:400-407.
50. Penhale P.A., Thayer G.W. Uptake and transfer of carbon and phosphorus by eelgrass (Zostera marina L.) and its epiphytes. J. Exp. Mar. Biol. Ecol. 1980, 42:113-123.
51. Perez M., Garcia T., Invers O., Ruiz J.M. Physiological responses of the seagrass Posidonia oceanica as indicators of fish farm impact. Mar. Pollut. Bull. 2008, 56:869-879.
52. Pergent-Martini C., Leoni V., Pasqualini V., Adrizzone G.D., Balestri E., Bedini R., Belluscio A., Belsher T., Borg J., Boudouresque C.F., Boumaza S., Bouquegneau J.M., Buia M.C., Calvo S., Cebrian J., Charbonnel E., Cinelli F., Cossu A., Di Maida G., Dural B., Francour P., Gobert S., Lepoint G., Meinesz A., Molenaar H., Mansour H.M., Panayotidis P., Peirano A., Pergent G., Piazzi L., Pirrotta M., Relini G., Romero J., Sanchez-Lizaso J.L., Semroud R., Shembri P., Shili A., Tomasello A., Velimirov B. Descriptors of Posidonia oceanica meadows: use and application. Ecol. Indic. 2005, 5:213-230.
53. Piazzi L., Balata D., Cinelli F., Benedetti-Cecchi L. Patterns of spatial variability in epiphytes of Posidonia oceanica: differences between a disturbed and two reference locations. Aquat. Bot. 2004, 79:345-356.
54. Pitta P., Apostolaki E.T., Tsagaraki T., Tsapakis M., Karakassis I. Fish farming effects on chemical and microbial variables of the water column: a spatio-temporal study along the Mediterranean Sea. Hydrobiologia 2006, 563:99-108.
55. Pitta P., Tsapakis M., Apostolaki E.T., Tsagaraki T., Holmer M., Karakassis I. 'Ghost nutrients' from fish farms are transferred up the food web by phytoplankton grazers. Mar. Ecol. Prog. Ser. 2009, 374:1-6.
56. Prado P., Alcoverro T., Martinez-Crego B., Verges A., Perez M., Romero J. Macrograzers strongly influence patterns of epiphytic assemblages in seagrass meadows. J. Exp. Mar. Biol. Ecol. 2007, 350:130-143.
57. Prado P., Alcoverro T., Romero J. Seasonal response of Posidonia oceanica epiphyte assemblages to nutrient increase. Mar. Ecol. Prog. Ser. 2008, 359:89-98.
58. Prado P., Romero J., Alcoverro T. Nutrient status, plant availability and seasonal forcing mediate fish herbivory in temperate seagrass beds. Mar. Ecol. Prog. Ser. 2010, 409:229-239.
59. Ruiz J.M., Marco-Mendez C., Sanchez-Lizaso J.L. Remote influence of off-shore fish farm waste on Mediterranean seagrass (Posidonia oceanica) meadows. Mar. Environ. Res. 2010, 69:118-126.
60. Ruiz J.M., Perez M., Romero J. Effects of fish farm loadings on seagrass (Posidonia oceanica) distribution, growth and photosynthesis. Mar. Pollut. Bull. 2001, 42:749-760.
61. Ruiz J.M., Perez M., Romero J., Tomas F. The importance of herbivory in the decline of a seagrass (Posidonia oceanica) meadow neaf a fish farm: An experimental approach. Bot. Mar. 2009, 52:449-458.
62. Santos R., Silva J., Alexandre A., Navarro N., Barron C., Duarte C.M. Ecosystem metabolism and carbon fluxes of a tidally-dominated coastal lagoon. Estuaries 2004, 27:977-985.
63. Strickland J.D., Parsons T.R. A practical handbook of sea-water analysis. Bull. Fish. Res. Board Can. 1972, 167:311.
64. Terrados J., Medina-Pons F.J. Epiphyte load on the seagrass Posidonia oceanica (L.) Delile does not indicate anthropogenic nutrient loading in Cabrera Archipelago National Park (Balearic Islands, Western Mediterranean). Sci. Mar. 2008, 72:503-510.
65. Tomasko D.A., Lapointe B.E. Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Mar. Ecol. Prog. Ser. 1991, 75:9-17.
66. Wetzel R.G., Penhale P.A. Transport of carbon and excretion of dissolved organic carbon by leaves and roots/rhizomes in seagrasses and their epiphytes. Aquat. Bot. 1979, 6:149-158.
67. Yarbro L.A., Carlson P.R. Community oxygen and nutrient fluxes in seagrass beds of Florida Bay, USA. Estuaries Coasts 2008, 31:877-897.
68. Ziegler S., Benner R. Dissolved organic carbon cycling in a subtropical seagrass-dominated lagoon. Mar. Ecol. Prog. Ser. 1999, 180:149-160.