Botanica Pacifica

Research paper

Botanica Pacifica. A journal of plant science and conservation 2020.9(2):61-72
Article first published online: 24 JUL 2020 | DOI: 10.17581/bp.2020.09207

Interspecific variation in foliar nutrients and isotopes of submerged macrophytes in the Cau Hai Lagoon, the typical brackish lagoon in Vientam

Dang Thi Nhu Y1,2, Nguyen Tien Hoang7, Pham Khac Lieu3, Hidenori Harada5, Keisuke Koba4, Natacha Brion6, Duong Van Hieu8, Nguyen Van Hop8, Tim Sierens1 & Harry Olde Venterink1

1 Department of Biology, Vrije Universiteit Brussel (VUB), Brussels, Belgium
2 VNUK Institute for Research and Executive Education, The University of Danang, Danang, Vietnam
3 Department of Science, Technology and Environment, Hue University, Hue, Vietnam
4 Center for Ecological Research, Kyoto University, Otsu, Shiga 520–2113, Japan
5 Graduate School of Global Environmental Studies, Kyoto University, Kyoto 606–8501, Japan
6 Analytical, Environmental and Geochemistry, Vrije Universiteit Brussel (VUB), Brussels, Belgium
7 Laboratory of Environmental Geosphere Engineering, Department of Urban Management, Graduate School of Engineering, Kyoto University, Kyoto 615–8540, Japan
8 College of Sciences, Hue University, Hue, Vietnam

Submersed macrophytes are key elements of shallow coastal ecosystems but globally declined due to anthropogenic disturbances and climate change. Foliar elemental and isotopic compositions of macrophytes are being increasingly used to identify nutritional status and environmental conditions including potential stress factors, thereto insight is required in its interspecific variation. In this paper, we present interspecific variations in foliar nutrients (C, N, P) and stable isotopes (δ13C and δ15N) of four macrophyte species (Najas indica, Halophila beccarii, Halodule uninervis, Halophila ovalis) in Cau Hai lagoon (Vietnam) in relation to key environmental variables. The foliar C, N, δ13C and δ15N values varied among species and related to salinity, water depth and/or DIN concentrations. Foliar N and C:N values were correlated to DIN concentration in the water (N. indica and H. beccarii, respectively), whereas foliar C:P was correlated to P concentrations in sediment (N. indica) or water depth (H. uninervis). Foliar δ13C of H. beccarii and H. uninervis increased with salinity and δ15N of N. indica with both salinity and DIN concentration in the water. These aquatic plants likely varied either in resource acquisition strategies (e.g. uptake of CO2 or HCO3–, N and P from different sources) or in their usage (e.g. C investment in structural tissue) and in their response to changes in salinity, water depth and DIN concentration in the water. The studied macrophytes likely experienced relatively high N and P availability and another factor than P or N probably inhibited C-fixation and/or carbon storage of these plants.

Данг Ти Нху И, Нгуен Тиен Хоанг, Фам Хак Лию, Харада Х., Коба К., Брион Н., Ван Хью Д., Ван Хоп Н., Сиренз Т., Вентеринк Г.О. Межвидовая изменчивость листовых питательных веществ и изотопов погруженных видов макрофитов в лагуне Кау Хай - типичной солоноватой лагуне Вьетнама. Погруженные макрофиты являются ключевыми компонентами мелководных прибрежных экосистем. В глобальном масштабе их сообщества существенно сократились из-за антропогенных нарушений и изменения климата. Элементные и изотопные составы листьев макрофитов все чаще используются для определения их пищевого статуса и условий окружающей среды, включая потенциальные стрессовые факторы, для чего необходимо понимание их межвидовой изменчивости. В настоящей работе мы представляем результаты исследования межвидовых вариаций внекорневых питательных веществ (C, N, P) и стабильных изотопов (δ13C и δ15N) четырех видов макрофитов: Najas indica, Halophila beccarii, Halodule uninervis, Halophila ovalis в лагуне Кау-Хай (Вьетнам) в зависимости от ключевых переменных окружающей среды. Содержания C, N, значения δ13C и δ15N варьировали в зависимости от вида и были связаны с соленостью, глубиной воды и/или концентрацией DIN. Содержание N и значения C:N коррелировали с концентрацией DIN в воде у N. indica и H. beccarii, тогда как значения C:P коррелировали с концентрацией P в детрите (N. indica) или в толще воды (H. uninervis). δ13C у H. beccarii и H. uninervis увеличивалась с повышением солености, а δ15N у N. indica – как с повышением солености, так и с концентрацией DIN в воде. Макрофиты различались в стратегиях потребления ресурсов (например, поглощение CO2 или HCO3–, N и P из различных источников), в их использовании (например, инвестиции C в структурные ткани), а также по их реакции на изменения солености, глубины воды и концентрации DIN в воде. Изученные макрофиты находились в условиях доступности N и P, а фиксация С ингибировалась другими факторами..

Keywords: Najas, Halophila, Halodule, salinity, depth, DIN, phosphorus, соленость, глубина, фосфор

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References

Andersen, J.M. 1976. An ignition method for determination of total phosphorus in lake sediments. Water Research 10: 329-331. CrossRef

Anderson, W.T. & J.W. Fourqurean 2003. Intra- and interannual variability in seagrass carbon and nitrogen stable isotopes from south Florida, a preliminary study. Organic Geochemistry 34: 185-194. CrossRef

APHA: American Public Health Association 1999. Standard Methods for the Examination of Water and Wastewater, 20th edition. American Public Health Association, American Water Works Association, Water Environment Federation, Washington DC.

Apostolaki, E.T., M. Holmer, N. Marbà & I. Karakassis 2011. Reduced carbon sequestration in a Mediterranean seagrass (Posidonia oceanica) ecosystem impacted by fish farming. Aquaculture Environment Interactions 2:49-59. CrossRef

Atkinson, M. & S. Smith 1983. C:N:P ratios of benthic marine plants. Limnology and Oceanography 28: 568-574. CrossRef

Beer, S., M. Bjork, F. Hellblom & L. Axelsson 2002. Inorganic carbon utilization in marine angiosperms (seagrasses). Functional Plant Biology 29:349-354. CrossRef

Borum, J., O. Pedersen, L. Kotula, M.W. Fraser, J. Statton, T.D. Colmer & G.A. Kendrick 2016. Photosynthetic response to globally increasing CO2 of co-occurring temperate seagrass species. Plant, Cell and Environment 39:1240-1250. CrossRef

Burkholder, J.M., D.A. Tomasko & B.W. Touchette 2007. Seagrasses and eutrophication. Experimental Marine Biology and Ecology 350:46-72. CrossRef

Campbell, J.E. & J.W. Fourqurean 2009. Interspecific variation in the elemental and stable isotope content of seagrasses in South Florida. Marine Ecology Progress Series 387: 109-123. CrossRef

Campbell, J.E. & J.W. Fourqurean 2013. Mechanisms of bicarbonate use influence the photosynthetic carbon dioxide sensitivity of tropical seagrasses. Limnology and Oceanography 58:839-848. CrossRef

Cao, V.L., V.T. Nguyen, T. Komatsu, D.V. Nguyen & D.T. Dam 2012. Status and threats on seagrass beds using GIS in Vietnam. SPIE-Remote Sensing of the Marine Environment II. p. 8525 12. Last accessed 20.09.2019. CrossRef

Carlson, R.E. 1977. A trophic state index for lakes. Limnology and Oceanography 22:361-369. CrossRef

Chappuis, E., V. Seriñá, E. Martí, E. Ballesteros & E. Gacia 2017. Decrypting stable isotope (δ13C and δ15N) variability in aquatic plants. Freshwater Biology 62(11):1-12. CrossRef

Connolly, R.M., D. Gorman, J.S. Hindell, T.N. Kildea & T.A. Schlacher 2013. High congruence of isotope sewage signals in multiple marine taxa. Marine Pollution Bulletin 71: 152-158. CrossRef

Daya A.A. & H. Bejari 2015. A comparative study between simple kriging and ordinary kriging for estimating and modeling the Cu concentration in Chehlkureh deposit, SE Iran. Arabian Journal of Geosciences 8:6003-6020. CrossRef

Disperati, L. & S.G.P. Virdis 2015. Assessment of land-use and land-cover changes from 1965 to 2014 in Tam Giang-Cau Hai Lagoon, central Vietnam. Applied Geography 58: 48-64. CrossRef

Duarte, C.M. 1990. Seagrass nutrient content. Marine Ecology Progress Series 67:201-201. CrossRef

Estefan, G., R. Sommer & J. Ryan 2014. Analytical Methods for Soil, Plant and Water in the Dry Areas: A manual of Relevance to the West Asia and North Africa Region, Third Edition. nternational Center for Agriculture research in the Dry Areas, Aleppo, 255 pp.

Falkowski, G.D. Farquhar, J.R. Ehleringer & K.T. Hubick 1989. Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40:503-537. CrossRef

Ferdie, M. & J.W. Fourqurean 2004. Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnology and Oceanography 49:2082-2094. CrossRef

Fourqurean, J.W., S.A. Manuel, K.A. Coates, W.J. Kenworthy & J.N. Boyer 2015. Water quality, isoscapes and stoichioscapes of seagrasses indicate general P limitation and unique N cycling in shallow water benthos of Bermuda. Biogeosciences 12:6235-6249. CrossRef

Fourqurean, J.W., N. Marba, C.M. Duarte, E. Diaz-Almela & S. Ruiz-Halpern 2007. Spatial and temporal variation in the elemental and stable isotopic content of the seagrasses Posidonia oceanica and Cymodocea nodosa from the Illes Balears, Spain. Marine Biology 151:219-232. CrossRef

Fourqurean, J.F., T.O. Moore, B. Fry & J.T. Hollibaugh 1997. Spatial and temporal variation in C:N:P ratios, δ15N, and δ13C of eelgrass Zostera marina as indicators of ecosystem processes, Tomales Bay, California, USA. Marine Ecology Progress Series 157:147-157. CrossRef

Fraser, M.W., G.A. Kendrick, P.F. Grierson, J.W. Fourqurean, M.A. Vanderklift & D.I. Walker 2012. Nutrient status of seagrasses cannot be inferred from system-scale distribution of phosphorus in Shark Bay, Western Australia. Marine and Freshwater Research 63:1015-1026. CrossRef

Fry, B. 2002. Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries and Coasts 25:264-271. CrossRef

Geovariances 2016. ISATIS Software: Technical References Release 2016.1. Geovariances & Ecole des Mines de Paris, Paris, France.

Goovaerts, P. 1997. Geostatistics for Natural Resources Evaluation. Oxford University Press, New York.

Gordon, D.M., P.B. Birch & A.J. McComb 1981. Effects of inorganic phosphorus and nitrogen on the growth of an estuarine Cladophora in culture. Botanica Marina 24: 93-106. CrossRef

Gorman, D., A. Turra, R.M. Connolly, A.D. Olds & T.A. Schlacher 2017. Monitoring nitrogen pollution in seasonally-pulsed coastal waters requires judicious choice of indicator species. Marine Pollution Bulletin 122:149-155. CrossRef

Hemminga, M.A. & M.A. Mateo 1996. Stable carbon isotopes in seagrass: variability in ratios and use in ecological studies. Marine Ecology 140:285-298. CrossRef

Herbeck, L.S., M. Sollich, D. Unger, M. Holmer & T.C. Jennerjahn 2014. Impact of pond aquaculture effluents on seagrass performance in NE Hainan, tropical China. Marine Pollution Bulletin 85:190-203. CrossRef

Hitchcock, J.K., S.C. Courtenay, M.R.S. Coffin, C.C. Pater & M.R. van Den Heuvel 2017. Eelgrass bed structure, leaf nutrient, and leaf isotope responses to natural and anthropogenic gradients in estuaries of the Southern Gulf of St. Lawrence, Canada. Estuaries and Coasts 40:1653-1665. CrossRef

Hobbie, E., A. Jumpponen & J. Trappe 2005. Foliar and fungal 15N:14N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models. Oecologia 146:258-268. CrossRef

Hoyer, M.V., T.K Frazer., S.K. Notestein & D.E. Canfield 2004. Vegetative characteristics of three low-lying Florida coastal rivers in relation to flow, light, salinity and nutrients. Hydrobiologia 528:31-43. CrossRef

Invers, O., M. Perez & J. Romero 1999. Bicarbonate utilization in seagrass photosynthesis: role of carbonic anhydrase in Posidonia oceanica (L) Delile and Cymodocea nodosa (Ucria) Ascherson. Journal of Experimental Marine Biology and Ecology 235:125-133. CrossRef

Johengen, T. 1997. Standard operating procedures for determining total phosphorus, available phosphorus, and biogenic silica concentrations of Lake Michigan sediments and sediment trap material, in Lake Michigan mass balance study (LMMB) methods compendium. In: Metals, conventionals, radiochemistry and biomonitoring sample analysis techniques, vol. 3, (L. Blume, ed.), pp. 305-312, United States Environmental Protection Agency (EPA 905R97012c).

Johnson, M.W., K.L Heck & J.W. Fourqurean 2006. Nutrient content of seagrasses and epiphytes in the northern Gulf of Mexico: Evidence of phosphorus and nitrogen limitation. Aquatic Botany 85:103-111. CrossRef

Keeley, J.E. & D.R. Sandquist 1992. Carbon: freshwater plants. Plant, Cell and Environment 15:1021-1035. CrossRef

Kratzer, C.R. & P.L. Brezonik 1981. A carlson-type trophic state index for nitrogen in florida lakes. Water Resources Bulletin 17:713-715. CrossRef

Le, X.T. 2012. Preliminary assessment of sea level rise impacts to coastal ecosystems in Thua Thien-Hue. VNU Journal of Science, Earth Sciences 28:140-151.

Lepoint, G., P. Dauby & S. Gobert 2004. Applications of C and N stable isotopes to ecological and environmental studies in seagrass ecosystems. Marine Pollution Bulletin 49: 887-891. CrossRef

Lepoint, G., B. Frederich, S. Gobert & E. Parmentier 2008. Isotopic ratios and elemental contents as indicators of seagrass C processing and sewage influence in a tropical macrotidal ecosystem (Madagascar, Mozambique Channel). Scientia Marina 72:109-117. CrossRef

Logan, M. 2010. Biostatistical design and analysis using R: A practical guide. Wiley & Blackwell, England, 557 pp. CrossRef

Michener, R.H. & K. Lajtha 2007. Stable isotopes in ecology and environmental science. Blackwell Scientific Publications, Oxford, 592 pp. CrossRef

Mook, W.G. 2000. Environmental isotopes in the hydrological cycle: principles and applications, vol. 1: Introduction; theory, methods, review. IHP-V Technical documents in hydrology. No 39, Vol. I. UNESCO, Paris.

Murphy, J. & J.P. Riley 1962. A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta 27:31-36. CrossRef

Nguyen, Q.C.T. & M. Yabe 2014. Shrimp poly-culture development and local livelihoods in Tam Giang-Cau Hai Lagoon, Vietnam. Agricultural Science 6:1-14. CrossRef

Odelu, G., N.M. Kumar, N. Siddulu & K. Raghu 2014. Enumeration of macrophytes of eutrophicated and noneutrophicated lakes of two tahasils of Karim Nagar District. Biolife 2:1170-1180.

Oksanen, J., G.F. Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B. O'Hara, G.L. Simpson, P. Solymos, M.H.H. Stevens & H. Wagner 2013. vegan: Community Ecology Package. R package version 2.0-9. Available at http://cran.rproject.org/package=vegan.

Paerl, H 2009. Controlling eutrophication along the freshwater - marine continuum: dual nutrient (N and P) reductions are essential. Estuaries and Coasts 32:593-601. CrossRef

Peipoch, M., E. Gacia, A. Blesa, M. Ribot, J.L. Riera & E. Martí 2014. Contrasts among macrophyte riparian species in their use of stream water nitrate and ammonium: insights from 15N natural abundance. Aquatic Sciences 76:203-215. CrossRef

Phan, T.T.H. 2018. Submerged aquatic vegetation in a tropical lagoon environment: Dynamics and resilience strategy. PhD thesis, Vrije Universiteit Brussels, Belgium. 193 pp.

R Core Team 2017. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Raven, J.A., A.M Johnston, J.E Kübler, R. Korb, S.G. McInroy, L.L. Handley, C.M. Scrimgeour, D.I. Walker, J. Beardall, M. Vanderklift, S. Fredriksen & K.H. Dunton 2002. Mechanistic interpretation on carbon isotope by marine macroalgae and seagrasses. Functional Plant Biology 29:355-378. CrossRef

Risk, M.J., B.E. Lapointe, O.A. Sherwood & B.J. Bedford 2009. The use of δ15N in assessing sewage stress on coral reefs. Marine Pollution Bulletin 58:793-802. CrossRef

Schmidt, A.L., J.K.C. Wysmyk, S.E. Craig & H.K. Lotze 2012. Regional-scale effects of eutrophication on ecosystem structure and services of seagrass beds. Limnology and Oceanography 57:1389-1402. CrossRef

Schwarz, A.M., M. Björk, T. Buluda, H. Mtolera & S. Beer 2000. Photosynthetic utilisation of carbon and light by two tropical seagrass species as measured in situ. Marine Biology 137:755-761. CrossRef

Shilla, D.A., T. Asaeda, S. Kian, R. Lalith & J. Manatunge 2006. Phosphorus concentration in sediment, water and tissues of three submerged macrophytes of Myall Lake, Australia. Wetlands Ecology and Management 14:549-558. CrossRef

Short, F.T., B. Polidoro, S.R. Livingstone, K.E. Carpenter, S. Bandeira, J.S. Bujang, H.P. Calumpong, T.J.B. Carruthers, R.G. Coles, W.C. Dennison, P.L.A Erftemeijer, M.D. Fortes, A.S. Freeman, T.G. Jagtap, A.H.M. Kamal, G.A. Kendrick, W. Judson Kenworthy , Y.A. La Nafie, I.M. Nasution, R.J. Orth, A. Prathep, J.C. Sanciangco, B. van Tussenbroek, S.G. Vergara, M. Waycott & J.C. Zieman 2011. Extinction risk assessment of the world's seagrass species. Biological Conservation 144:1961-1971. CrossRef

Schmidt, M., H.S. Windisch, K.U. Ludwichowski, S.L.L. Seegert, H.O. Portner, D. Storch & C. Bock 2018. Seawater carbonate chemistry and neurochemical profiles of two gadid species. PANGAEA. https://doi.org/10.1594/PANGAEA.892312.

Stapel, J. & M.A. Hemminga 1997. Nutrient resorption from seagrass leaves. Marine Biology 128:197-206. CrossRef

Sun, Z., X. Mou, X. Li, L. Wang, H. Song & H. Jiang 2011. Application of stable isotope techniques in studies of carbon and nitrogen biogeochemical cycles of ecosystem. Chinese Geographical Science 21:129-148. CrossRef

Thanh, T.D., Y. Saito, V.D. Huy, V.L. Nguyen, T.K.O. Ta & M. Tateishi 2004. Regimes of human and climate changes in Vietnam. Regional Environmental Change 4:49-62. CrossRef

Udy, U.W & W.C. Dennison 1997. Growth and physiological responses of three seagrass species to elevated sediment nutrients in Moreton Bay, Australia. Experimental Marine Biology and Ecology 217:253-277. CrossRef

Uku, J., S. Beer & M. Bjork 2005. Buffer sensitivity of photosynthetic carbon utilisation in eight tropical seagrasses. Marine Biology 147:1085-1090. CrossRef

Van Katwijk, M.M., M.E.W. Van der Welle, E.C.H.E.T. Lucassen, J.A. Vonk, M.J.A. Christianen, K.W. HakimI, A. Arifin, T.J. Bouma, J.G.M. Roelofs & L.P.M. Lamers 2011. Early warning indicators for river nutrient and sediment loads in tropical seagrass beds: a benchmark from a nearpristine archipelago in Indonesia. Marine Pollution Bulletin 62:1512-1520. CrossRef

Vizzini, S. & A. Mazzola 2004. Stable isotope evidence for the environmental impact of a land-based fish farm in the western Mediterranean. Marine Pollution Bulletin 49: 61-70. CrossRef

Walton, M.E.M., I. Al-Maslamani, N. Haddaway, H. Kennedy & A. Castillo 2016. Extreme 15N depletion in seagrasses. Estuaries and Coasts 39:1709-1723. CrossRef

Waycott, M., C.M. Duarte, T.J.B. Carruthers, R.J. Orth, W.C. Dennison, S. Olyarnik, A. Calladine, J.W. Fourqurean,K.L. Heck Jr., A. Randall Hughes, G.A. Kendrick, W.J. Kenworthy, F.T. Short & S.L. Williams 2006. Accelerating loss of seagrasses across the Globe threatens coastal ecosystems. PNAS 106(30):12377-12381. CrossRef

West, J.B., G.J. Bowen, T.E. Cerling & J.R. Ehleringer 2006. Stable isotopes as one of nature's ecological recorders. Trends in Ecology and Evolution 21:408-414. CrossRef

Whalen, M.A., J.E. Duffy & J.B. Grace 2013. Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology 94:510-520. CrossRef

Yamamuro, M., H. Kayanne & H. Yamano 2003. δ15N of seagrass leaves for monitoring anthropogenic nutrient increases in coral reef ecosystems. Marine Pollution Bulletin 46:452-458. CrossRef

Yu, H., Z. Yu, X. Song, X. Cao, Y. Yuan & G. Lu 2015. Seasonal variations in the nitrogen isotopic composition of dissolved nitrate in the Changjiang River estuary, China. Estuarine, Coastal and Shelf Science 155:148-155. CrossRef





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