Abstract
Cymodocea nodosa, a typical marine angiosperm species in the Mediterranean Sea, hosts a range of epiphytic algae. Epiphyte abundance varies at different spatial scales, yet epiphyte diversity and community composition are poorly understood. This study explores the epiphytes on C. nodosa from two reference meadows (Thasos, Vrasidas) and one anthropogenically stressed meadow (Nea Karvali) in the northern Aegean Sea (Kavala Gulf, Greece). A nested destructive sampling design at three spatial scales (metres, hundreds of metres, kilometres) and stereoscopic/microscopic observations were used. Light microscopy revealed a total of 19 taxa of macroalgae populating the leaves of C. nodosa. The most commonly encountered taxa with highest cover (%) were Hydrolithon cruciatum and Feldmannia mitchelliae. DNA sequencing (18S rDNA) confirms the presence of a number of dinoflagellate and red algal epiphytes, and this represents the first application of DNA metabarcoding to study the diversity of seagrass epiphytes. Epiphytic communities studied at species/taxon and functional (Ecological Status Groups) levels separated the reference low-stressed meadows from the degraded one, with the functional approach having higher success. The ecological evaluation index classified the studied meadows into different Ecological Status Classes according to anthropogenic stress.
Funding source: UK Natural Environment Research Council
Award Identifier / Grant number: NE/D521522/1
Award Identifier / Grant number: NE/J023094/1
Funding source: Molecular Genetics Facility
Award Identifier / Grant number: MGF 154
About the authors
Soultana Tsioli is a final year PhD biologist at the National and Kapodistrian University of Athens, Greece. Her research interests focus on ecophysiology of seagrasses, the impacts of global climate changes on seagrasses and systematics of seaweeds. The epiphytes of Cymodocea across an eutrophication gradient have been studied during her diploma thesis.
Dr. Vasillis Papathanasiou is a researcher at the Fisheries Research Institute, Nea Peramos, Greece. He has worked on the use of macrophytes as bioindicators of ecological quality and the development of monitoring protocols and programs. He has focused on the experimental study of stress factors and climate change scenarios on seagrasses and their distribution. He worked on the mapping and monitoring of seagrasses.
Dr. Eva Papastergiadou is a Professor of Ecology at the Department of Biology, University of Patras, Greece with an expertise in ecosystem-scale dynamics, aquatic macrophytes ecology, functional diversity patterns and processes of aquatic assemblages. She has experience as key partner and national representative of Greece and Cyprus in WFD intercalibration process, in many national and international projects, organization of workshops, and coordination of scientific working teams. She is an editorial board member of five international journals, and an editor of two journal special issues.
Dr. Frithjof C. Küpper holds a chair in Marine Biodiversity at the University of Aberdeen, studying the biodiversity and biochemistry of marine plants/algae. His research found that iodide serves as an inorganic antioxidant in kelp, the first known from a living system, impacting atmospheric and marine chemistry. A certified scientific diver, Frithjof has worked in the Mediterranean, South Atlantic (Ascension and Falklands), but also in the Antarctic and the Arctic for algal diversity-related projects.
Dr. Sotiris Orfanidis is a Research Director at Fisheries Research Institute specializing in the biodiversity of transitional and coastal waters benthic macrophytes and their ecophysiological interactions with the abiotic stress. Two biotic indices to assess water quality within the framework of European Water Directives were developed in his laboratory. He participated in National and European projects, (co)organized symposia and workshops, and is a handling editor of three international journals.
Acknowledgments
This work has been conducted at the Fisheries Research Institute (ELGO DIMITRA) as an undergraduate dissertation of Soultana Tsioli at the University of Patras with supervisors Prof. E. Papastergiadou and Dr. S. Orfanidis.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: FCK received funding from the UK Natural Environment Research Council (NERC, program Oceans 2025 – WP 4.5 and grants NE/D521522/1 and NE/J023094/1). Sequencing was conducted at the Molecular Genetics Facility (MGF) of NERC, supported by grant MGF 154.
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J.H., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402, https://doi.org/10.1093/nar/25.17.3389.Search in Google Scholar
Apostolaki, E.T., Holmer, M., Marbà, N., and Karakassis, I. (2011). Reduced carbon sequestration in a Mediterranean seagrass (Posidonia oceanica) ecosystem impacted by fish farming. Aquac. Environ. Interact. 2: 49–59, https://doi.org/10.3354/aei00031.Search in Google Scholar
Balata, D., Bertocci, I., Piazzi, L., and Nesti, U. (2008). Comparison between epiphyte assemblages of leaves and rhizomes of the seagrass Posidonia oceanica subjected to different levels of anthropogenic eutrophication. Estuar. Coast Shelf Sci. 79: 533–540, https://doi.org/10.1016/j.ecss.2008.05.009.Search in Google Scholar
Balata, D., Nesti, U., Piazzi, L., and Cinelli, F. (2007). Patterns of spatial variability of seagrass epiphytes in the north-west Mediterranean Sea. Mar. Biol. 151: 2025–2035, https://doi.org/10.1007/s00227-006-0559-y.Search in Google Scholar
Bartolo, A., Zammit, G., Peters, A.F., and Küpper, F.C. (2020). DNA barcoding of macroalgae in the Mediterranean Sea. Bot. Mar. 63: 253–272, https://doi.org/10.1515/bot-2019-0041.Search in Google Scholar
Ben Brahim, M., Mabrouk, L., Hamza, A., and Jribi, I. (2020). Comparison of spatial scale variability of shoot density and epiphytic leaf assemblages of Halophila stipulacea and Cymodocea nodosa on the Eastern Coast of Tunisia. Plant Biosyst. 154: 413–426, https://doi.org/10.1080/11263504.2019.1674399.Search in Google Scholar
Borowitzka, M.A., Lavery, P.S., and Van Keulen, M. (2006). Epiphytes of seagrasses. In: Larkum, A.W.D., Orth, R.J., and Duarte, C.M. (Eds.), Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp. 441–461.10.1007/978-1-4020-2983-7_19Search in Google Scholar
Borowitzka, M.A., Lethbridge, R.C., and Charlton, L. (1990). Species richness, spatial distribution and colonization pattern of algal and invertebrate epiphytes on the seagrass Amphibolis griffithii. Mar. Ecol. Prog. Ser. 64: 281–291, https://doi.org/10.3354/meps064281.Search in Google Scholar
Borum, J. (1985). Development of epiphytic communities on eelgrass (Zostera marina) along a nutrient gradient in a Danish estuary. Mar. Biol. 87: 211–218, https://doi.org/10.1007/bf00539431.Search in Google Scholar
Browne, C.M., Milne, R., Griffiths, C., Bolton, J.J., and Anderson, R.J. (2013). Epiphytic seaweeds and invertebrates associated with South African populations of the rocky shore seagrass Thalassodendron leptocaule — a hidden wealth of biodiversity. Afr. J. Mar. Sci. 35: 523–531, https://doi.org/10.2989/1814232x.2013.864332.Search in Google Scholar
Buia, M.C., Russo, G.F., and Mazzella, L. (1985). Inerrelazioni tra Cymodocea nodosa e Zostera noltii in un prato misto superficiale dell’ isola si Ischia. Nova Thalassia 7: 406–408.Search in Google Scholar
Cambridge, M.L., How, J.R., Lavery, P.S., and Vanderklift, M.A. (2007). Retrospective analysis of epiphyte assemblages in relation to seagrass loss in a eutrophic coastal embayment. Mar. Ecol. Prog. Ser. 346: 97–107, https://doi.org/10.3354/meps06993.Search in Google Scholar
Campbell, J.E. and Fourqurean, J.W. (2014). Ocean acidification outweighs nutrient effects in structuring seagrass epiphyte communities. J. Ecol. 102: 730–737, https://doi.org/10.1111/1365-2745.12233.Search in Google Scholar
Campbell, S.J., Mckenzie, L.J., and Kerville, S.P. (2006). Photosynthetic responses of seven tropical seagrasses to elevated seawater temperature. J. Exp. Mar. Biol. Ecol. 330: 455–468, https://doi.org/10.1016/j.jembe.2005.09.017.Search in Google Scholar
Cancemi, G., Buia, M.C., and Mazzella, L. (2002). Structure and growth dynamics of Cymodocea nodosa meadows. Sci. Mar. 66: 365–373.10.3989/scimar.2002.66n4365Search in Google Scholar
Carpenter, R.C. (1990). Competition among marine macroalgae: a physiological perspective. J. Phycol. 26: 6–12, https://doi.org/10.1111/j.0022-3646.1990.00006.x.Search in Google Scholar
Chung, M.-H. and Lee, K.-S. (2008). Species composition of the epiphytic diatoms on the leaf tissues of three Zostera species distributed on the southern coast of Korea. ALGAE 23: 75–81, https://doi.org/10.4490/algae.2008.23.1.075.Search in Google Scholar
Cloern, J.E. (2001). Our evolving conceptual model of the coastal eutrophication problem. Mar. Ecol. Prog. Ser. 210: 223–253, https://doi.org/10.3354/meps210223.Search in Google Scholar
Coleman, V.L. and Burkholder, J.M. (1995). Response of microalgal epiphyte communities to nitrate enrichment in an eelgrass (Zostera marina) meadow. J. Phycol. 31: 36–43, https://doi.org/10.1111/j.0022-3646.1995.00036.x.Search in Google Scholar
De Jonge, V.N., Elliott, M., and Orive, E. (2002). Causes, historical development, effects and future challenges of a common environmental problem: eutrophication. Nutrients and eutrophication in estuaries and coastal waters. Springer.10.1007/978-94-017-2464-7Search in Google Scholar
Dixon, L.K. (2000). Establishing light requirements for the seagrass Thalassia testudinum: an example from Tampa Bay, Florida. In: Bortone, S.A. (Ed.), Seagrasses: monitoring, ecology, physiology, and management. Bora Raton, Florida: CRC Marine Science Series.Search in Google Scholar
Doyle, J.J. and Doyle, J.L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Photochem. Bull. 19: 11–15.Search in Google Scholar
Duarte, C.M. (1995). Submerged aquatic vegetation in relation to different nutrient regimes. Ophelia 41: 87–112, https://doi.org/10.1080/00785236.1995.10422039.Search in Google Scholar
Fonseca, M.S., Fisher, J.S., Zieman, J.C., and Thayer, G.W. (1982). Influence of the seagrass, Zostera marina L., on current flow. Estuar. Coast Shelf Sci. 15: 351–358, https://doi.org/10.1016/0272-7714(82)90046-4.Search in Google Scholar
Frankovich, T.A., Armitage, A.R., Wachnicka, A.H., Gaiser, E.E., and Fourqurean, J.W. (2009). Nutrient effects on seagrass epiphyte community structure in Florida bay. J. Phycol. 45: 1010–1020, https://doi.org/10.1111/j.1529-8817.2009.00745.x.Search in Google Scholar
García-Redondo, V., Bárbara, I., and Díaz-Tapia, P. (2019). Biodiversity of epiphytic macroalgae (Chlorophyta, Ochrophyta, and Rhodophyta) on leaves of Zostera marina in the northwestern Iberian Peninsula. An. del Jardín Botánico Madr. 76: e078, https://doi.org/10.3989/ajbm.2502.Search in Google Scholar
Giovannetti, E., Montefalcone, M., Morri, C., Bianchi, C., and Albertelli, G. (2010). Early warning response of Posidonia oceanica epiphyte community to environmental alterations (Ligurian Sea, NW Mediterranean). Mar. Pollut. Bull. 60: 1031–1039, https://doi.org/10.1016/j.marpolbul.2010.01.024.Search in Google Scholar
Gobert, S., Sartoretto, S., Rico-Raimondino, V., Andral, B., Chery, A., Lejeune, P., and Boissery, P. (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, https://doi.org/10.1016/j.marpolbul.2009.06.012.Search in Google Scholar
Guiry, M.D., and Guiry, G.M. (2020). AlgaeBase. World-wide electronic publication. Galway, Ireland: National University of Ireland, http://www.algaebase.org.Search in Google Scholar
Hall, T.A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.Search in Google Scholar
Hamisi, M., Díez, B., Lyimo, T., Ininbergs, K., and Bergman, B. (2013). Epiphytic cyanobacteria of the seagrass Cymodocea rotundata: diversity, diel nifH expression and nitrogenase activity. Environ. Microbiol. Rep. 5: 367–376, https://doi.org/10.1111/1758-2229.12031.Search in Google Scholar
Heck, K.L., Pennock, J.R., Valentine, J.F., Coen, L.D., and Sklenar, S.A. (2000). Effects of nutrient enrichment and small predator density on seagrass ecosystems: an experimental assessment. Limnol. Oceanogr. 45: 1041–1057, https://doi.org/10.4319/lo.2000.45.5.1041.Search in Google Scholar
Hemminga, M.A. and Duarte, C.M. (2000). Seagrass ecology. Cambridge: Cambridge University Press.10.1017/CBO9780511525551Search in Google Scholar
Holmer, M. (2019). Productivity and biogeochemical cycling in seagrass ecosystems. In: Perillo, G.M.E., Wolanski, E., Cahoon, D.R., and Hopkinson, C.S. (Eds.), Coastal wetlands. Elsevier, chapter 13.10.1016/B978-0-444-63893-9.00013-7Search in Google Scholar
Irving, A.D. and Connell, S.D. (2006). Predicting understorey structure from the presence and composition of canopies: an assembly rule for marine algae. Oecologia 148: 491–502, https://doi.org/10.1007/s00442-006-0389-0.Search in Google Scholar
Jacobs, R., Hemerlink, P., and Van Geel, G. (1983). Epiphytic algae on eelgrass at Roscoff. France. Aquat. Bot. 15: 157–173, https://doi.org/10.1016/0304-3770(83)90026-8.Search in Google Scholar
Jernakoff, P., Brearley, A., and Nielsen, J. (1996). Factors affecting grazer-epiphyte interactions in temperate seagrass meadows. Oceanogr. Mar. Biol. 34: 109–162.Search in Google Scholar
Johnson, M.P., Edwards, M., Bunker, F., and Maggs, C.A. (2005). Algal epiphytes of Zostera marina: variation in assemblage structure from individual leaves to regional scale. Aquat. Bot. 82: 12–26, https://doi.org/10.1016/j.aquabot.2005.02.003.Search in Google Scholar
Küpper, F.C. and Kamenos, N.A. (2018). The future of marine biodiversity and marine ecosystem functioning in UK coastal and territorial waters (including UK Overseas Territories) – with an emphasis on marine macrophyte communities. Bot. Mar. 61: 521–535, https://doi.org/10.1515/bot-2018-0076.Search in Google Scholar
Kendrick, G.A. and Burt, J.S. (1997). Seasonal changes in epiphytic macro-algae assemblages between offshore exposed and inshore protected Posidonia sinuosa Cambridge et Kuo seagrass meadows. Western Australia 40: 77, https://doi.org/10.1515/botm.1997.40.1-6.77.Search in Google Scholar
Koch, E.W., Ackerman, J.D., Verduin, J., and Van Keulen, M. (2006). Fluid dynamics in seagrass ecology – from molecule to ecosystems. In: Larkum, A.W.D., Orth, R.J., and Duarte, C.M. (Eds.), Seagrasses: biology, ecology and conservation. Dordrecht: Springer.Search in Google Scholar
Larkum, A., Orth, R., and Duarte, C. (2006). Seagrasses: biology, ecology and conservation. The Netherlands: Springer.Search in Google Scholar
Larsson, A. (2014). AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30: 3276–3278, https://doi.org/10.1093/bioinformatics/btu531.Search in Google Scholar
Lavery, P.S. and Vanderklift, M.A. (2002). A comparison of spatial and temporal patterns in epiphytic macroalgal assemblages of the seagrasses Amphibolis griffithii and Posidonia coriacea. Mar. Ecol. Prog. Ser. 236: 99–112, https://doi.org/10.3354/meps236099.Search in Google Scholar
Littler, M.M., and Littler, D.S. (1980). The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am. Nat. 116: 25–44, https://doi.org/10.1086/283610.Search in Google Scholar
Marbà, N., Duarte, C.M., Alexandre, A., and Cabaço, S. (2004). How do seagrasses grow and spread? In: Borum, J., Duarte, C.M., Krause-Jensen, D., and Greve, T.M. (Eds.), European seagrasses: an introduction to monitoring and management. The M&MS project, pp. 11–18.Search in Google Scholar
Marin, B., Klingberg, M., and Melkonian, M. (1998). Phylogenetic relationships among the cryptophyta: analyses of nuclear-encoded SSU rRNA sequences support the monophyly of extant plastid-containing lineages. Protist 149: 265–276, https://doi.org/10.1016/s1434-4610(98)70033-1.Search in Google Scholar
Marin, B., Palm, A., Klingberg, M., and Melkonian, M. (2003). Phylogeny and taxonomic revision of plastid containing Euglenophytes based on SSU rDNA sequence comparisons and synapomorphic signatures in the SSU rRNA secondary structure. Protist 154: 99–145, https://doi.org/10.1078/143446103764928521.Search in Google Scholar
May, V. (1982). The use of epiphytic algae to indicate environmental changes. Aust. J. Ecol. 7: 101–102, https://doi.org/10.1111/j.1442-9993.1982.tb01305.x.Search in Google Scholar
May, V., Collins, A.J., and Collett, L.C. (1978). A comparative study of epiphytic algal communities on two common genera of seagrasses in eastern Australia. Aust. J. Ecol. 3: 91–104, https://doi.org/10.1111/j.1442-9993.1978.tb00855.x.Search in Google Scholar
Mazzella, L. and Spinoccia, L. (1992). Epiphytic diatoms of leaf blades of the Mediterranean seagrass Posidonia oceanica (L.) Delile. G. Bot. Ital. 126: 752–754, https://doi.org/10.1080/11263509209428168.Search in Google Scholar
Mazzella, L., Buia, M.C., and Spinoccia, L. (1994). Biodiversity of epiphytic diatom community on leaves of Posidonia oceanica. In: Marino, D., and Montresor, M. (Eds.), Proceedings 13th International Diatom Symposium. Biopress Limit, Bristol, pp. 241–251.Search in Google Scholar
Mcglathery, K.J., Sundbäck, K., and Anderson, I.C. (2007). Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter. Mar. Ecol. Prog. Ser. 348: 1–18, https://doi.org/10.3354/meps07132.Search in Google Scholar
Michael, T.S., Shin, H.W., Hanna, R., and Spafford, D.C. (2008). A review of epiphyte community development: surface interactions and settlement on seagrass. J. Environ. Biol. 29: 629–638.Search in Google Scholar
Moore, K.A. (2004). Influence of seagrasses on water quality in shallow regions of the lower Chesapeake bay. J. Coast Res: 162–178, https://doi.org/10.2112/si45-162.1.Search in Google Scholar
Ondiviela, B., Losada, I.J., Lara, J.L., Maza, M., Galván, C., Bouma, T.J., and Van Belzen, J. (2014). The role of seagrasses in coastal protection in a changing climate. Coast. Eng. 87: 158–168, https://doi.org/10.1016/j.coastaleng.2013.11.005.Search in Google Scholar
O’neill, R. (1988). Hierarchy theory and global change. In: Rosswall, T., W, R., and Risser, P.G. (Eds.), Scales and global change. John Wiley & Sons, New York, pp. 29–45.Search in Google Scholar
Orfanidis, S., Panayotidis, P., and Stamatis, N. (2001). Ecological evaluation of transitional and coastal waters: a marine benthic macrophytes-based model. Mediterr. Mar. Sci. 2: 45–65, https://doi.org/10.12681/mms.266.Search in Google Scholar
Orfanidis, S., Panayotidis, P., and Ugland, K. (2011). Ecological Evaluation Index continuous formula (EEI-c) application: a step forward for functional groups, the formula and reference condition values. Mediterr. Mar. Sci. 12: 34, https://doi.org/10.12681/mms.60.Search in Google Scholar
Orfanidis, S., Papathanasiou, V., Mittas, N., Theodosiou, T., Ramfos, A., Tsioli, S., Kosmidou, M., Kafas, A., Mystikou, A., and Papadimitriou, A. (2020). Further improvement, validation, and application of CymoSkew biotic index for the ecological status assessment of the Greek coastal and transitional waters. Ecol. Indic. 118: 106727, https://doi.org/10.1016/j.ecolind.2020.106727.Search in Google Scholar
Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck, K.L., Hughes, A.R., Kendrick, G.A., Kenworthy, W.J., Olyarnik, S., et al.. (2006). A global crisis for seagrass ecosystems. Bioscience 56: 987–996, https://doi.org/10.1641/0006-3568(2006)56[987:agcfse]2.0.co;2.10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2Search in Google Scholar
Papathanasiou, V. and Orfanidis, S. (2018). Anthropogenic eutrophication affects the body size of Cymodocea nodosa in the North Aegean Sea: a long-term, scale-based approach. Mar. Pollut. Bull. 134: 38–48, https://doi.org/10.1016/j.marpolbul.2017.12.009.Search in Google Scholar
Papathanasiou, V., Orfanidis, S., and Brown, M.T. (2015). Intra-specific responses of Cymodocea nodosa to macro-nutrient, irradiance and copper exposure. J. Exp. Mar. Biol. Ecol. 469: 113–122, https://doi.org/10.1016/j.jembe.2015.04.022.Search in Google Scholar
Pardi, G., Piazzi, L., Balata, D., Papi, I., Cinelli, F., and Benedetti-Cecchi, L. (2006). Spatial variability of Posidonia oceanica (L.) Delile epiphytes around the mainland and the islands of Sicily (Mediterranean Sea). Mar. Ecol. 27: 397–403, https://doi.org/10.1111/j.1439-0485.2006.00099.x.Search in Google Scholar
Pergent, G., Bazairi, H., Bianchi, C.N., Boudouresque, C., Buia, M., Calvo, S., Clabaut, P., Harmelinvivien, M., Angel Mateo, M., and Montefalcone, M. (2014). Climate change and Mediterranean seagrass meadows: a synopsis for environmental managers. Mediterr. Mar. Sci. 15: 462–473, https://doi.org/10.12681/mms.621.Search in Google Scholar
Piazzi, L., Balata, D., Cinelli, F., and Benedetti-Cecchi, L. (2004). Patterns of spatial variability in epiphytes of Posidonia oceanica: differences between a disturbed and two reference locations. Aquat. Bot. 79: 345–356, https://doi.org/10.1016/j.aquabot.2004.05.006.Search in Google Scholar
Piazzi, L., Balata, D., and Ceccherelli, G. (2016). Epiphyte assemblages of the Mediterranean seagrass Posidonia oceanica: an overview. Mar. Ecol. 37: 3–41, https://doi.org/10.1111/maec.12331.Search in Google Scholar
Piazzi, L., De Biasi, A., Balata, D., Pardi, G., Boddi, S., Acunto, S., Pertusati, M., Papi, I., Cinelli, F., and Sartoni, G. (2007). Species composition and spatial variability patterns of morphological forms in macroalgal epiphytic assemblages of the seagrass Posidonia oceanica. Vie Milieu 57: 171.Search in Google Scholar
Prado, P. (2018). Seagrass epiphytic assemblages are strong indicators of agricultural discharge but weak indicators of host features. Estuar. Coast Shelf Sci. 204: 140–148, https://doi.org/10.1016/j.ecss.2018.02.026.Search in Google Scholar
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., and Glöckner, F.O. (2013). The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41: D590–D596, https://doi.org/10.1093/nar/gks1219.Search in Google Scholar
R Core Team (2020). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.Search in Google Scholar
Reyes, J. and Sanson, M. (1997). Temporal distribution and reproductive phenology of the epiphytes on Cymodocea nodosa leaves in the Canary Islands. Bot. Mar. 40: 193–201, https://doi.org/10.1515/botm.1997.40.1-6.193.Search in Google Scholar
Reyes, J. and Sansón, M. (2001). Biomass and production of the epiphytes on the leaves of Cymodocea nodosa in the Canary Islands. Bot. Mar. 44: 307–313, https://doi.org/10.1515/bot.2001.039.Search in Google Scholar
Ruiz-Frau, A., Gelcich, S., Hendriks, I.E., Duarte, C.M., and Marbà, N. (2017). Current state of seagrass ecosystem services: research and policy integration. Ocean Coast. Manage. 149: 107–115, https://doi.org/10.1016/j.ocecoaman.2017.10.004.Search in Google Scholar
Saunders, J.E., Attrill, M.J., Shaw, S.M., and Rowden, A.A. (2003). Spatial variability in the epiphytic algal assemblages of Zostera marina seagrass beds. Mar. Ecol. Prog. Ser. 249: 107–115, https://doi.org/10.3354/meps249107.Search in Google Scholar
Schramm, W. (1999). Factors influencing seaweed responses to eutrophication: some results from EU-project EUMAC. J. Appl. Phycol. 11: 69, https://doi.org/10.1023/a:1008076026792.10.1007/978-94-011-4449-0_72Search in Google Scholar
Schramm, W. and Nienhuis, P. (1996). Marine benthic vegetation: recent changes and the effects of eutrophication. Springer Science & Business Media.10.1007/978-3-642-61398-2Search in Google Scholar
Short, F.T. and Burdick, D.M. (1996). Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts. Estuaries 19: 730–739, https://doi.org/10.2307/1352532.Search in Google Scholar
Stankovic, M., Tantipisanuh, N., and Prathep, A. (2018). Carbon storage in seagrass ecosystems along the Andaman coast of Thailand. Bot. Mar. 61: 429–440, https://doi.org/10.1515/bot-2017-0101.Search in Google Scholar
Surek, B., Beemelmanns, U., Melkonian, M., and Bhattacharya, D. (1994). Ribosomal RNA sequence comparisons demonstrate an evolutionary relationship between Zygnematales and charophytes. Plant Syst. Evol. 191: 171–181, https://doi.org/10.1007/bf00984663.Search in Google Scholar
Tomasko, D. and Lapointe, B. (1991). 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. 75: 9–17, https://doi.org/10.3354/meps075009.Search in Google Scholar
Trautman, D.A. and Borowitzka, M.A. (1999). Distribution of the epiphytic organisms on Posidonia australis and P. sinuosa, two seagrasses with differing leaf morphology. Mar. Ecol. Prog. Ser. 179: 215–229, https://doi.org/10.3354/meps179215.Search in Google Scholar
Trevathan-Tackett, S.M., Kelleway, J., Macreadie, P.I., Beardall, J., Ralph, P., and Bellgrove, A. (2015). Comparison of marine macrophytes for their contributions to blue carbon sequestration. Ecology 96: 3043–3057, https://doi.org/10.1890/15-0149.1.Search in Google Scholar
Tsioli, S., Orfanidis, S., Papathanasiou, V., Katsaros, C., and Exadactylos, A. (2019). Effects of salinity and temperature on the performance of Cymodocea nodosa and Ruppia cirrhosa: a medium-term laboratory study. Bot. Mar. 62: 97–108, https://doi.org/10.1515/bot-2017-0125.Search in Google Scholar
Turki, S. (2005). Distribution of toxic dinoflagellates along the leaves of seagrass Posidonia oceanica and Cymodocea nodosa from the Gulf of Tunis. Cah. Biol. Mar. 46: 29–34.Search in Google Scholar
Uku, J. and Björk, M. (2001). The distribution of epiphytic algae on three Kenyan seagrass species. S. Afr. J. Bot. 67: 475–482, https://doi.org/10.1016/s0254-6299(15)31166-2.Search in Google Scholar
Van Der Ben, D. (1971). Les épiphytes des feuilles de Posidonia oceanica Delile sur les côtes françaises de la Méditerranée, Vol. 168. Mémoires Institut Royal des Sciences Naturelles de Belgique.Search in Google Scholar
Vanderklift, M.A. and Lavery, P.S. (2000). Patchiness in assemblages of epiphytic macroalgae on Posidonia coriacea at a hierarchy of spatial scales. Mar. Ecol. Prog. Ser. 192: 127–135, https://doi.org/10.3354/meps192127.Search in Google Scholar
Yilmaz, P., Parfrey, L.W., Yarza, P., Gerken, J., Pruesse, E., Quast, C., Schweer, T., Peplies, J., Ludwig, W., and Glöckner, F.O. (2013). The SILVA and “All-species living tree project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42: D643–D648, https://doi.org/10.1093/nar/gkt1209.Search in Google Scholar
Supplementary Material
The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2020-0057).
© 2021 Walter de Gruyter GmbH, Berlin/Boston
