The Second Skin of Seagrass Leaves: A Comparison of Microalgae Epiphytic Communities Between Two Different Species Across Two Seagrass Meadows in Lesser Sunda Islands
Main Article Content
Abstract
Epiphytes as the important features in the seagrass ecosystems have been studied widely, and their functions as a primary producer, influence rates of herbivory grazer, and prevent seagrass leaf from desiccation is well known. However, patterns and distribution among seagrasses especially in Indonesia, which was known as hotspot marine biodiversity is not well understood. Therefore, this study aimed to examined epiphytic assemblages on two seagrass species with different morphological and longevity, Enhalus acoroides and Cymodocea rotundata, in two different meadows (conservation area and non-conservation area) in Lesser Sunda Islands (Bali and Lombok). A total of 22 taxa of microalgae epiphytes species were identified from eight sites and 2 different species of seagrass. The highest number of collected species between class was from Bacillariophyceae (18), followed by Cyanophyceae (3) and Fragilariophyceae (1). Analysis of similarity (ANOSIM) revealed a significant difference of microalgae epiphytes assemblages between sites and seagrasses. Epiphytes assemblages in conservation area were more abundant than non-conservation area, both in Bali and Lombok. On seagrass comparison, Enhalus acoroides showed higher abundance of epiphytes assemblages than those on Cymodocea rotundata. Based on principal component analysis (PCA), this study highlights the microalgae epiphytic communities strongly influenced by seawater temperature, phosphate’s concentration, and pH in sediment. This study also demonstrated that the assemblages of microalgae epiphytic communities affected by differences of seagrass morphological and longevity.
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
Aho K and Beck E. (2011). Effects of epiphyte cover on seagrass growth rates in two tidal zones. Dartmouth Undergraduate Journal of Science 2011: 43–44.
Anderson M J and Walsh D C. (2013). PERMANOVA, ANOSIM, and the Mantel Test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecological Monograph 83(4): 557–574. https://doi.org/10.1890/12-2010.1
Balata D, Nesti U, Piazzi L and Cinelli F. (2007). Patterns of spatial variability of seagrass epiphytes in the north-west Mediterranean Sea. Marine Biology 151(6): 2025–2035. https://doi.org/10.1007/s00227-006-0559-y
Ben Brahim M, Hamza A, Hannachi I, Rebai A, Jarboui O, Bouain A and Aleya L. (2010). Variability in the structure of epiphytic assemblages of Posidonia Oceanica in relation to human interferences in the Gulf of Gabes, Tunisia. Marine Environmental Research 70(5): 411–421. https://doi.org/10.1016/j.marenvres.2010.08.005
Brodersen K E, Koren K, Revsbech N P and Kühl M. (2020). Strong leaf surface basification and CO2 limitation of seagrass induced by epiphytic biofilm microenvironments. Plant Cell and Environment 43(1): 174–187. https://doi.org/10.1111/pce.13645
Brouns J W M. (1987). Growth patterns in some indo-west-pacific seagrasses. Aquatic Botany 28(1): 39–61. https://doi.org/10.1016/0304-3770(87)90055-6
Burkholder J M, Tomasko D A and Touchette B W. (2007). Seagrasses and eutrophication. Journal of Experimental Marine Biology and Ecology 350: 46–72. https://doi.org/10.1016/j.jembe.2007.06.024
Campbell J E and Fourqurean J W. (2014). Ocean acidification outweighs nutrient effects in structuring seagrass epiphyte communities. Journal of Ecology 102: 730–737. https://doi.org/10.1111/1365-2745.12233
Cheng C C. (2004). Statistical approaches on discriminating spatial variation of species diversity. Botanical Bulletin of Academia Sinica 45(4): 339–346. https://doi.org/10.7016/BBAS.200410.0339
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(1): 75–81. https://doi.org/10.4490/algae.2008.23.1.075
Clarke K R. (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18(1): 117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Coll M, Schmidt A, Romanuk T and Lotze H K. (2011). Food-web structure of seagrass communities across different spatial scales and human impacts. PLoS ONE 6(7): e22591. https://doi.org/10.1371/journal.pone.0022591
Corlett H and Jones B. (2007). Epiphyte communities on Thalassia testudinum from Grand Cayman, British West Indies: Their composition, structure, and contribution to lagoonal sediments. Sedimentary Geology 194(3–4): 245–262. https://doi.org/10.1016/j.sedgeo.2006.06.010
Cornelisen C D and Thomas F I M. (2004). Ammonium and nitrate uptake by leaves of the seagrass Thalassia testudinum: Impact of hydrodynamic regime and epiphyte cover on uptake rates. Journal of Marine Systems 49(1–4): 177–194. https://doi.org/10.1016/j.jmarsys.2003.05.008
Crump B C and Koch E W. (2008). Attached bacterial populations shared by four species of aquatic angiosperms. Applied and Environmental Microbiology 74(19): 5948–5957. https://doi.org/10.1128/AEM.00952-08
Daby D. (2003). Effects of seagrass bed removal for tourism purposes in a Mauritian Bay. Environmental Pollution 125(3): 313–324. https://doi.org/10.1016/S0269-7491(03)00125-8
Duarte C M. (2000). Marine biodiversity and ecosystem services: An elusive link. Journal of Experimental Marine Biology and Ecology 250(1–2): 117–131. https://doi.org/10.1016/S0022-0981(00)00194-5
Enríquez S and Pantoja-Reyes N I. (2005). Form-function analysis of the effect of canopy morphology on leaf self-shading in the seagrass Thalassia testudinum. Oecologia 145(2): 235–243. https://doi.org/10.1007/s00442-005-0111-7
Fourqurean J W, Muth M F and Boyer J N. (2010). Epiphyte loads on seagrasses and microphytobenthos abundance are not reliable indicators of nutrient availability in oligotrophic coastal ecosystems. Marine Pollution Bulletin 60(7): 971–983. https://doi.org/10.1016/j.marpolbul.2010.03.003
Gartner A, Tuya F, Lavery P S and McMahon K. (2013). Habitat preferences of macroinvertebrate fauna among seagrasses with varying structural forms. Journal of Experimental Marine Biology and Ecology 439: 143–151. https://doi.org/10.1016/j.jembe.2012.11.009
Güre?en A, Güre?en S O and Aktan Y. (2020). Temporal and bathymetric variation of epiphytic microalgae on Posidonia oceanica (L.) delile leaves in Gökçeada (North Aegean, Turkey). Turkish Journal of Fisheries and Aquatic Sciences 20(10): 727–737. https://doi.org/10.4194/1303-2712-v20_10_02
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. Environmental Microbiology Reports 5(3): 367–376. https://doi.org/10.1111/1758-2229.12031
Harrison P G and Durance C D. (1985). Reductions in photosynthetic carbon uptake in epiphytic diatoms by water-soluble extracts of leaves of Zostera marina. Marine Biology 90(1): 117–119. https://doi.org/10.1007/BF00428222
Heck K L, Pennock J, 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. Limnology and Oceanography 45(5): 1041–1057. https://doi.org/10.3354/meps07442
Hoang H T T, Duong T T, Nguyen K T, Le Q T P, Luu M T N, Trinh D A and Le A H. (2018). Impact of anthropogenic activities on water quality and plankton communities in the day river (Red River Delta, Vietnam). Environmental Monitoring and Assessment 190: 67. https://doi.org/10.1007/s10661-017-6435-z
Hoppenrath M, Elbrachter M and Drebes G. (2009). Marine phytoplankton: Selected microphytoplankton species from the North Sea around Helgoland and Sylt, Kleine Senckenberg-Reihe 49. Stuttgart, Germany: E. Schweizerbart’sche Verlagsbuchhandlung.
Houk P and Camacho R. (2010). Dynamics of seagrass and macroalgal assemblages in Saipan Lagoon, Western Pacific Ocean: Disturbances, pollution, and seasonal cycles. Botanica Marina 53(3): 205–212. https://doi.org/10.1515/BOT.2010.025
Joung S H, Oh H M, Ko S R and Ahn C Y. (2011). Correlations between environmental factors and toxic and non-toxic microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10(2): 188–193. https://doi.org/10.1016/j.hal.2010.09.005
Karlina I, Kurniawan F and Idris F. (2018). Pressures and status of seagrass ecosystem in the coastal areas of North Bintan, Indonesia. E3S Web of Conferences 47: 1–6. https://doi.org/10.1051/e3sconf/20184704008
Kocak F and Aydin-Onen S. (2014). Epiphytic bryozoan community of Posidonia oceanica (L.) delile leaves in two different meadows at disturbed and control locations. Mediterranean Marine Science 15(2): 390–397. https://doi.org/10.12681/mms.777
Lapointe B E, Barile P J and Matzie W R. (2004). Anthropogenic nutrient enrichment of seagrass and coral reef communities in the lower Florida keys: Discrimination of local versus regional nitrogen sources. Journal of Experimental Marine Biology and Ecology 308(1): 23–58. https://doi.org/10.1016/j.jembe.2004.01.019
Larink O and Westheide W. (2006). Coastal plankton: Photo guide for European Sea. Germany: Alfred Wegener Institute for Polar and Marine Research Munchen.
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. Marine Ecology Progress Series 236: 99–112. https://doi.org/10.3354/meps236099
Lavery P S, Reid T, Hyndes G A and Van Elven B R. (2007). Effect of leaf movement on epiphytic algal biomass of seagrass leaves. Marine Ecology Progress Series 338: 97–106. https://doi.org/10.3354/meps338097
Lebreton B, Richard P, Radenac G, Bordes M, Bréret M, Arnaud C, Mornet F and Blanchard G F. (2009). Are epiphytes a significant component of intertidal Zostera noltii beds? Aquatic Botany 91(2): 82–90. https://doi.org/10.1016/j.aquabot.2009.03.003
Leliaert F, Van reusel W, Clerck O D E and Coppejans E. (2001). Epiphytes on the seagrasses of Zanzibar Island (TANZANIA), floristic and ecological aspects. Belgian Journal of Botany 134(1): 3–20.
Lobelle D, Kenyon E J, Cook K J and Bull J C. (2013). Local competition and metapopulation processes drive long-term seagrass-epiphyte population dynamics. PLoS ONE 8(2): e57072. https://doi.org/10.1371/journal.pone.0057072
Mabrouk L, Brahim M B, Hamza A, Mahfoudhi M and Bradai M N. (2014). A comparison of abundance and diversity of epiphytic microalgal assemblages on the leaves of the seagrasses Posidonia oceanica (L.) and Cymodocea nodosa (Ucria) asch in Eastern Tunisia. Journal of Marine Biology 2014: 275305. https://doi.org/10.1155/2014/275305
Marco-Méndez C, Ferrero-Vicente L M, Prado P, Heck K L, Cebrián J and Sánchez-Lizaso J L. (2015). Epiphyte presence and seagrass species identity influence rates of herbivory in Mediterranean seagrass meadows. Estuarine, Coastal and Shelf Science 154: 94–101. https://doi.org/10.1016/j.ecss.2014.12.043
Medlin L K and Juggins S. (2018). Multivariate analyses document host specificity, differences in the diatom metaphyton vs. epiphyton, and seasonality that structure the epiphytic diatom community. Estuarine, Coastal and Shelf Science 213: 314–330. https://doi.org/10.1016/j.ecss.2018.06.011
Nelson W G. (2017). Development of an epiphyte indicator of nutrient enrichment: Threshold values for seagrass epiphyte load. Ecological Indicators 74: 343–356. https://doi.org/10.1016/j.ecolind.2016.11.035
Odum E O. (1971). Fundamental of Ecology. 2nd Ed. Philadelphia: W. B. Saunders.
Olds A D, Connolly R M, Pitt K A, Pittman S J, Maxwell P S, Huijbers C M and Moore B R. (2016). Quantifying the conservation value of seascape connectivity: A global synthesis. Global Ecology and Biogeography 25(1): 3–15. https://doi.org/10.1111/geb.12388
Orbita M L S and Mukai H. (2013). Relationship between epiphytes and the photosynthetic activity of temperate seagrasses. Advances in Agriculture & Botanics-International Journal of the Bioflux Society [AAB Bioflux] 5(3): 163–168. http://www.aab.bioflux.com.ro
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). Marine Ecology 27(4): 397–403. https://doi.org/10.1111/j.1439-0485.2006.00099.x
Piazzi L, Balata D and Ceccherelli G. (2016). Epiphyte assemblages of the Mediterranean seagrass Posidonia oceanica: An overview. Marine Ecology 37(1): 3–41. https://doi.org/10.1111/maec.12331
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. Aquatic Botany 79(4): 345–356. https://doi.org/10.1016/j.aquabot.2004.05.006
Prabakaran M. (2011). Invitro antimicrobial potentials of Marine Oscillatoria species. Asian Journal of Plant Science and Research 1(3): 58–64.
Prado P, Alcoverro T, Martínez-Crego B, Vergés A, Pérez M and Romero J. (2007). Macrograzers strongly influence patterns of epiphytic assemblages in seagrass meadows. Journal of Experimental Marine Biology and Ecology 350(1–2): 130–143. https://doi.org/10.1016/j.jembe.2007.05.033
Rattanachot E and Prathep A. (2011). Temporal variation in growth and reproduction of Enhalus acoroides (L.f.) royle in a monospecific meadow in Haad Chao Mai National Park, Trang Province, Thailand. Botanica Marina 54: 201–207. https://doi.org/10.1515/BOT.2011.018
Reyes J and Sanson M. (2001). Biomass and production of the epiphytes on the leaves of Cymodocea nodosa in the Canary Islands. Botanica Marina 44: 307–13. https://doi.org/10.1515/BOT.2001.039
Shaffai, A E. (2011). Seagrasses of the Red Sea. First edit. Switzerland: IUCN. https://portals.iucn.org/library/efiles/edocs/2011-057.pdf
Short F T and Coles R G. (2001). Global seagrass research method. Amsterdam: Elsevier B.V.
Ugarelli K, Laas P and Stingl U. (2018). The microbial communities of leaves and roots associated with turtle grass (Thalassia testudinum) and manatee grass (Syringodium filliforme) are distinct from seawater and sediment communities, but are similar between species and sampling sites. Microorganisms 7(1): 4. https://doi.org/10.3390/microorganisms7010004
Uku J, Björk M, Bergman B and Díez B. (2007). Characterization and comparison of prokaryotic epiphytes associated with three East African seagrasses. Journal of Phycology 43(4): 768–779. https://doi.org/10.1111/j.1529-8817.2007.00371.x
Wear D J, Sullivan M J, Moore A D and Millie D F. (1999). Effects of water-column enrichment on the production dynamics of three seagrass species and their epiphytic algae. Marine Ecology Progress Series 179: 201–213. https://doi.org/10.3354/meps179201
Whalen M A, Duffy J E and Grace J B. (2013). Temporal shifts in top-down vs. bottomup control of epiphytic algae in a seagrass ecosystem. Ecology 94(2): 510–520. https://doi.org/10.1890/12-0156.1
Wirachwong P and Holmer M. (2010). Nutrient dynamics in 3 morphological different tropical seagrasses and their sediments. Aquatic Botany 93(3): 170–178. https://doi.org/10.1016/j.aquabot.2010.06.004