Marine Biology

, Volume 144, Issue 4, pp 653–664 | Cite as

Factors affecting macroalgal distribution in a eutrophic tropical lagoon in Taiwan

  • Hsing-Juh LinEmail author
  • Jia-Jang Hung
Research Article


Factors affecting distribution of macroalgal periphyton were examined during a complete seasonal cycle in Tapong Bay, a eutrophic tropical lagoon in southern Taiwan. Water residence time varied from a few days to weeks. Total biomass and species richness declined with increasing residence time. However, they appeared to exhibit a unimodal seasonal pattern across all study sites, with blooms and greater richness in winter and spring and lower values in summer and fall. Nonmetric multidimensional scaling ordination of macroalgal communities reveals a clear gradual continuum of changes in species composition along the flushing gradient, suggesting the communities were primarily structured by site, and secondarily by season. The fast-flushing region was dominated by the chlorophycean genus Ulva, which was replaced by Enteromorpha intestinalis at mid-flushing levels, while the cyanobacterium Lyngbya majuscula was the dominant species in the slow-flushing region. Tissue nitrogen, but not tissue phosphorus, of these dominant species increased with increasing nutrient availability as a result of slow flushing. Our results suggest that water motion was an important selective factor for the spatial dominance of macroalgal species in Tapong Bay. This study demonstrates that species-dependent ordination is more sensitive in discriminating between sites than are species-independent measures such as total biomass and nutrient content when monitoring coastal eutrophication in the tropics. However, more-sensitive ordination provides only an ‘early warning’ that a community is changing; less-sensitive measures are also required to indicate the magnitude and type of these environmental changes.


Phytoplankton Macroalgae Dissolve Organic Nitrogen Water Residence Time Herbivorous Fish 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was supported by the National Science Council under grant number NSC89-2621-2-056A-001. We are grateful to Miss Hui-Ying Wang and Miss Pei-Chen Wen for field and laboratory assistance. Comments by two anonymous reviewers were particularly helpful in revising the manuscript.


  1. Björnsäter BR, Wheeler PA (1990) Effect of nitrogen and phosphorus supply on growth and tissue composition of Ulva fenestrate and Enteromorpha intestinalis (Ulvales, Chlorophyta). J Phycol 26:603–611Google Scholar
  2. Borum J (1985) Development of epiphytic communities on eelgrass (Zostera marina) along a nutrient gradient in a Danish estuary. Mar Biol 87:211–218Google Scholar
  3. Chen J-N (2002) Numerical modeling of primary productivity in Tapong Bay. Master’s thesis, National Sun Yat-sen University, KaohsiungGoogle Scholar
  4. Clarke KR, Gorley RN (2001) PRIMER v5: user manual/tutorial. PRIMER-E, Plymouth, UKGoogle Scholar
  5. Clarke KR, Warwick RM (1994) Changes in marine communities: an approach to statistical analysis and interpretation. Natural Environment Research Council, Plymouth, UKGoogle Scholar
  6. Corredor JE, Howarth RW, Twilley RR, Morell JM (1999) Nitrogen cycling and anthropogenic impact in the tropical interamerican seas. Biogeochemistry 46:163–178Google Scholar
  7. Costanzo SD, O’Donohue MJ, Dennison WC (2000) Gracilaria edulis (Rhodophyta) as a biological indicator of pulsed nutrients in oligotrophic waters. J Phycol 36:680–685Google Scholar
  8. Diaz MR, Corredor JE, Morell JM (1990) Nitrogenase activity of Microcoleus lyngbyaceus mat communities in a eutrophic tropical marine environment. Limnol Oceanogr 35:1788–1795Google Scholar
  9. Downing JA, McClain M, Twilley RJ, Melack M, Elser J, Rabalais NN, Lewis WM, Turner RE Jr, Corredor J, Soto D, Yanez-Arancibia A, Kopaska JA, Howarth RW (1999) The impact of accelerating land-use change on the N-cycle of tropical aquatic ecosystems: current conditions and projected changes. Biogeochemistry 46:109–148CrossRefGoogle Scholar
  10. Erftemeijer PLA, Herman PMJ (1994) Seasonal changes in environmental variables, biomass, production and nutrient contents in two contrasting tropical intertidal seagrass beds in South Sulawesi, Indonesia. Oecologia 99:45–59Google Scholar
  11. Fong P, Boyer KE, Zedler JB (1998) Developing an indicator of nutrient enrichment in coastal estuaries and lagoons using tissue nitrogen content of the opportunistic alga, Enteromorpha intestinalis (L. Link). J Exp Mar Biol Ecol 231:63–79CrossRefGoogle Scholar
  12. Harlin MM (1995) Changes in major plant groups following nutrient enrichment. In: McComb AJ (ed) Eutrophic shallow estuaries and lagoons. CRC Press, Boca Raton, Fla., pp 173–187Google Scholar
  13. Hatcher BG, Larkum AWD (1983) An experimental analysis of factors controlling the standing crop of the epilithic algal community on a coral reef. J Exp Mar Biol Ecol 113:39–59Google Scholar
  14. Hein M, Pedersen MF, Sand-Jensen K (1995) Size-dependent nitrogen uptake in micro- and macroalgae. Mar Ecol Prog Ser 118:247–253Google Scholar
  15. Hernández I, Peralta G, Pérez-Lloréns JL, Vergara JJ, Niell FX (1997) Biomass and dynamics of growth of Ulva species in Palmones River estuary. J Phycol 33:764–772Google Scholar
  16. Horner RR, Welch EB (1981) Stream periphyton development in relation to current velocity and nutrients. Can J Fish Aquat Sci 38:449–457Google Scholar
  17. Horrocks JL, Stewart GR, Dennison WC (1995) Tissue nutrient content of Gracilaria spp. (Rhodophyta) and water quality along an estuarine gradient. Mar Freshw Res 46:975–983Google Scholar
  18. Huang SF (1990) The marine algal flora of Hsiao-Liuchiu Island. Bot Bull Acad Sinica 32:245–255Google Scholar
  19. Huang SF (1999) Floristic studies on the benthic marine algae of northeastern Taiwan. Taiwania 44:271–298Google Scholar
  20. Hughes TP, Szmant AM, Steneck R, Carpenter R, Miller S (1999) Algal blooms on coral reef: what are the causes? Limnol Oceanogr 44:1583–1586Google Scholar
  21. Hung P-Y (2001) Biogeochemical processes and fluxes of carbon and nutrients in the Tapong Bay. Master’s thesis, National Sun Yat-sen University, KaohsiungGoogle Scholar
  22. Jen P-H (2002) Tidal exchange process at Tapong Bay. Master’s thesis, National Sun Yat-sen University, KaohsiungGoogle Scholar
  23. Kaehler S, Williams GA (1996) Distribution of algae on tropical rocky shores: spatial and temporal patterns of non-coralline encrusting algae in Hong Kong. Mar Biol 125:177–187Google Scholar
  24. Kamer K, Boyl KA, Fong P (2001) Macroalgal bloom dynamics in a highly eutrophic southern California estuary. Estuaries 24:623–635Google Scholar
  25. Knoppers B, Kjerfve B, Carmouse JP (1991) Trophic state and water turn-over time in six choked coastal lagoons in Brazil. Biogeochemistry 14:149–166Google Scholar
  26. Kuffner IB, Paul VJ (2001) Effects of nitrate, phosphate and iron on the growth of macroalgae and benthic cyanobacteria from Cocos Lagoon, Guam. Mar Ecol Prog Ser 222:63–72Google Scholar
  27. Lapointe BE (1997) Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida. Limnol Oceanogr 42:1119–1131Google Scholar
  28. Lin H-J, Nixon SW, Taylor DI, Granger SL, Buckley BA (1996) Responses of epiphytes on eelgrass, Zostera marina L., to separate and combined nitrogen and phosphorus enrichment. Aquat Bot 52:243–258CrossRefGoogle Scholar
  29. Littler MM, Littler DS (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae: field and laboratory tests of a functional form model. Am Nat 116:25–44CrossRefGoogle Scholar
  30. Lowthion D, Soulsby PG, Houston MCM (1985) Investigation of a eutrophic tidal basin: part 1—factors affecting the distribution and biomass of macroalgae. Mar Environ Res 15:263–284CrossRefGoogle Scholar
  31. Lyngby JE, Mortensen SM (1994) Assessment of nutrient availability and limitation using macroalgae. J Aquat Ecosyst Health 3:27–34Google Scholar
  32. Martins I, Oliveira JM, Flindt MR, Marques JC (1999) The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecol 20:259–265CrossRefGoogle Scholar
  33. McIntire CD (1966) Some effects of current velocity on periphyton communities in laboratory streams. Hydrobiologia 27:559–570Google Scholar
  34. Naldi M, Viaroli P (2002) Nitrate uptake and storage in the seaweed Ulva rigida C. Agardh in relation to nitrate availability and thallus nitrate content in a eutrophic coastal lagoon (Sacca di Goro, Po River Delta, Italy). J Exp Mar Biol Ecol 269:65–83Google Scholar
  35. Nixon SW (1995) Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia 41:199–219Google Scholar
  36. Nixon SW, Ammerman JW, Atkinson LP, Berounsky VM, Billen G, Boicourt WC, Boynton WR, Church TM, Ditoro DM, Elmgren R, Garber JH, Giblin AE, Jahnke RA, Owens NJP, Pilson MEQ, Seitzinger SP (1996) The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry 35:141–180Google Scholar
  37. Osborne NJT, Webb PM, Shaw GR (2001) The toxins of Lyngbya majuscula and their human and ecological health effects. Environ Int 27:381–392PubMedGoogle Scholar
  38. Paerl HW, Fitzpatrick M, Bebout BM (1996) Seasonal nitrogen fixation dynamics in a marine microbial mat: potential roles of cyanobacteria and microheterotrophs. Limnol Oceanogr 41:419–427Google Scholar
  39. Pai SC, Yang CC, Riley JP (1990) Formation kinetics of the pink azo dye in the determination of nitrite in natural waters. Anal Chem Acta 232:345–349Google Scholar
  40. Peters G, Paznokas W, Noyes V (1985) A review of nutrient standards for the coastal lagoons in the San Diego region. San Diego region draft report. California Regional Water Quality Control Board, San Diego, Calif.Google Scholar
  41. Pregnall AM, Rudy PP (1985) Contribution of green macroalgal mats (Enteromorpha spp.) to seasonal production in an estuary. Mar Ecol Prog Ser 24:167–176Google Scholar
  42. Ridal JJ, Moore RM (1990) A re-examination of the measurement of dissolved organic phosphorus in seawater. Mar Chem 29:19–31Google Scholar
  43. Smith SV (1984) Phosphorus versus nitrogen limitation in the environment. Limnol Oceanogr 29:1149–1160Google Scholar
  44. Solorzano L, Sharp JH (1980) Determination of total dissolved phosphorus and particulate in natural waters. Limnol Oceanogr 25:754–758Google Scholar
  45. Souchu P, Vaquer A, Collos Y, Landrein S, Deslous-Paoli J-M, Bibent B (2001) Influence of shellfish farming activities on the biogeochemical composition of the water column in Thau lagoon. Mar Ecol Prog Ser 218:141–152Google Scholar
  46. Strickland JD, Parsons TR (1972) A practical handbook of seawater analysis, 2nd edn. Fisheries Research Board of Canada, OttawaGoogle Scholar
  47. Thacker RW, Paul VJ (2001) Are benthic cyanobacteria indicators of nutrient enrichment? Relationships between cyanobacterial abundance and environmental factors on the reef flats of Guam. Bull Mar Sci 69:497–508Google Scholar
  48. Traaen TS, Lindstrøm E-A (1983) Influence of current velocity on periphyton distribution. In: Wetzel RG (ed) Periphyton of freshwater ecosystems. Junk, The Hague, pp 97–99Google Scholar
  49. Valiela I, McClelland J, Hauxwell J, Behr PJ, Hersh D, Foreman K (1997) Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences. Limnol Oceanogr 42:1105–1118Google Scholar
  50. Vollenweider RA (1976) Advances in defining critical loading levels of phosphorus in lake eutrophication. Mem Ist Ital Idrobiol 33:53–58Google Scholar
  51. Wheeler PA, Björnsäter BR (1992) Seasonal fluctuations in tissue nitrogen, phosphorus, and N:P for five macroalgal species common to the Pacific northwest coast. J Phycol 28:1–6Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Life SciencesNational Chung Hsing UniversityTaichungTaiwan, R.O.C.
  2. 2.Institute of Marine Geology and ChemistryNational Sun Yat-sen UniversityKaohsiungTaiwan, R.O.C.

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