, Volume 818, Issue 1, pp 177–191 | Cite as

Assessing phytoplankton composition and structure within micro-estuaries and micro-outlets: a community analysis approach

  • Tatenda Dalu
  • Mandla L. Magoro
  • Jonathan D. Tonkin
  • Lucienne R. D. Human
  • Renzo Perissinotto
  • Shaun H. P. Deyzel
  • Janine B. Adams
  • Alan K. Whitfield
Primary Research Paper


Micro-estuaries and micro-outlets represent small coastal waterbodies that differ in their relative salinity and size, with the former being larger, more saline (mesohaline versus oligohaline), and exchanging with the sea more often than the latter. There are thousands of these waterbodies along the world’s coastline, yet few of these very small systems have been identified and studied. We investigated systematic differences between micro-estuaries and micro-outlets in terms of phytoplankton community composition, including spatio-temporal variation in both community structure and biomass (chlorophyll-a). A multivariate analysis was used to assess differences in environmental variables, biomass and phytoplankton community composition across four seasons and the two waterbody types. A total of 260 (63 families) and 244 (74 families) phytoplankton taxa were identified within the micro-estuaries and micro-outlets, respectively. Nano- and picoplankton were the dominant groups in micro-estuaries, and pico- and microplankton in micro-outlets. Micro-estuaries were rich in phytoplankton taxa representative of marine, estuarine and freshwater conditions, with a successional sequence in dominance evident, from Chlorophyta during winter to Bacillariophyta in spring and Cyanophyta in summer. By contrast, micro-outlets were mostly dominated by freshwater taxa, with Chlorophyta remaining the dominant group across all four seasons. Higher phytoplankton biomass was recorded during the winter when increased nutrients were available following catchment flooding. Seasonal switching in phytoplankton was reflected not only in changing dominance patterns in both habitat types but also in complete replacement of some species in micro-outlets, despite Chlorophyta remaining dominant. Such temporal turnover, which is often accompanied by predictable seasonal changes in environmental conditions, can promote overall species richness by allowing more taxa to coexist in a single environment through temporal niche segregation.


Biomass Chlorophyll-a Micro-estuaries Micro-outlets Phytoplankton Salinity 



The study was funded by the National Research Foundation (NRF), South African Institute for Aquatic Biodiversity (SAIAB) and Nelson Mandela University (NMU). Any opinions, findings, conclusions or recommendations expressed in this material are those of the authors, and the NRF, SAIAB and NMU do not accept any liability in this regard.

Supplementary material

10750_2018_3605_MOESM1_ESM.pdf (325 kb)
Supplementary material 1 (PDF 324 kb)


  1. Abbate, M. C. L., J. C. Molinero, V. A. Guinder, G. M. Perillo, R. H. Freije, U. Sommer, C. V. Spetter & J. E. Marcovecchio, 2017. Time-varying environmental control of phytoplankton in a changing estuarine system. Science of the Total Environment 609: 1390–1400.CrossRefGoogle Scholar
  2. Adams, J. B. & G. C. Bate, 1999. Primary producers—Estuarine microalgae. In Allanson, B. & D. Baird (eds), Estuaries of South Africa. Cambridge University Press, Cambridge.Google Scholar
  3. Allanson, B. R. & D. Baird (eds), 1999. Estuaries of South Africa. Cambridge University Press, Cambridge.Google Scholar
  4. Anandraj, A., R. Perissinotto & C. Nozais, 2007. A comparative study of microalgal production in a marine versus a river-dominated temporarily open/closed estuary, South Africa. Estuarine, Coastal and Shelf Science 73: 768–780.CrossRefGoogle Scholar
  5. Anandraj, A., R. Perissinotto, C. Nozais & D. Stretch, 2008. The recovery of microalgal production and biomass in a South African temporarily open/closed estuary, following mouth breaching. Estuarine, Coastal and Shelf Science 79: 599–606.CrossRefGoogle Scholar
  6. Anderson, M. J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.Google Scholar
  7. Anderson, M. J. & C. J. F. ter Braak, 2003. Permutation tests for multi-factorial analysis of variance. Journal of Statistical Computation and Simulation 73: 85–113.CrossRefGoogle Scholar
  8. Anderson, M. J., R. N. Gorley & K. R. Clarke, 2008. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth.Google Scholar
  9. Bate, G. C. & B. V. Heelas, 1975. Studies on the nitrate nutrition of two indigenous Rhodesian grasses. Journal of Applied Ecology 12: 941–952.CrossRefGoogle Scholar
  10. Bate, G. C., M. Nunes, B. Escott, A. Mnikathi & J. Craigie, 2017. Micro-estuary—a new estuary type recognised for South African conditions. Transactions of the Royal Society of South Africa 72: 85–92.CrossRefGoogle Scholar
  11. Dalu, T. & P. W. Froneman, 2016. Diatom based water quality monitoring in Africa: challenges and future prospects. Water SA 42: 551–559.CrossRefGoogle Scholar
  12. Dalu, T., P. W. Froneman & N. B. Richoux, 2014. Phytoplankton community diversity along a river–estuary continuum. Transactions of the Royal Society of South Africa 69: 107–116.CrossRefGoogle Scholar
  13. Dalu, T., N. B. Richoux & P. W. Froneman, 2016. Distribution of benthic diatom communities in a permanently open temperate estuary, in relation to physico-chemical variables. South African Journal of Botany 107: 31–38.CrossRefGoogle Scholar
  14. Dalu, T., J. B. Adams, J. C. Taylor, G. C. Bate, M. Nunes, P. W. Froneman & R. J. Wasserman, 2018. An overview of the ecology and status of estuarine microphytobenthos research in South Africa. African Journal of Marine Science 40: 1–12.CrossRefGoogle Scholar
  15. Demers, S., J. C. Therriault, E. Bourget & A. Bah, 1987. Resuspension in the shallow sublittoral zone of a macrotidal estuarine environment: wind influence. Limnology and Oceanography 32: 327–339.CrossRefGoogle Scholar
  16. Domingues, R. B., A. B. Barbosa, U. Sommer & H. M. Galvão, 2011. Ammonium, nitrate and phytoplankton interactions in a freshwater tidal estuarine zone: potential effects of cultural eutrophication. Aquatic Sciences 73: 331–343.CrossRefGoogle Scholar
  17. Du, Y., L. Yang & S. P. Xie, 2011. Tropical Indian Ocean influence on northwest Pacific tropical cyclones in summer following strong El Niño. Journal of Climate 24: 315–322.CrossRefGoogle Scholar
  18. Fisher, T. R., L. W. Harding Jr., D. W. Stanley & L. G. Ward, 1988. Phytoplankton, nutrients, and turbidity in the Chesapeake, Delaware, and Hudson estuaries. Estuarine, Coastal and Shelf Science 27: 61–93.CrossRefGoogle Scholar
  19. Fonge, A. B., B. G. Chuyong, A. S. Tening, A. C. Fobid & N. F. Numbisi, 2013. Seasonal occurrence, distribution and diversity of phytoplankton in the Douala Estuary. Cameroon, African Journal of Aquatic Science 38: 123–133.CrossRefGoogle Scholar
  20. Hensley, R. T. & M. J. Cohen, 2017. Flow reversals as a driver of ecosystem transition in Florida’s springs. Freshwater Science 36: 14–25.CrossRefGoogle Scholar
  21. Hilmer, T. & G. C. Bate, 1991. Vertical migration of a flagellate-dominated bloom in a shallow South African estuary. Botanica Marina 34: 113–121.CrossRefGoogle Scholar
  22. Hinga, K. R., 2002. Effects of pH on coastal marine phytoplankton. Marine Ecology Progress Series 238: 281–300.CrossRefGoogle Scholar
  23. Human, L. R. D., M. Magoro, T. Dalu, R. Perissinotto, A. K. Whitfield, J. B. Adam, S. H. P. Deyzel & G. M. Rishworth, 2018. Natural enrichment in pristine micro-estuaries and micro-outlets. Science of the Total Environment 624: 945–954.CrossRefPubMedGoogle Scholar
  24. Janse van Vuuren, S. & J. C. Taylor, 2015. Changes in the algal composition and water quality of the Sundays River, Karoo, South Africa, from source to estuary. African Journal of Aquatic Science 40: 339–357.CrossRefGoogle Scholar
  25. John, D., B. Whitton & A. Brook (eds), 2002. The freshwater algal flora of the British Isles: an identification guide to freshwater and terrestrial algae. Cambridge University Press, Cambridge.Google Scholar
  26. Ke, Z. X., Y. H. Tan, L. M. Huang, J. L. Zhang & S. M. Lian, 2012. Relationship between phytoplankton composition and environmental factors in the surface waters of southern South China Sea in early summer of 2009. Acta Oceanologica Sinica 31: 109–119.CrossRefGoogle Scholar
  27. Ke, Z., Y. Tan, Y. Ma, L. Huang & S. Wang, 2014. Effects of surface current patterns on spatial variations of phytoplankton community and environmental factors in Sunda shelf. Continental Shelf Research 82: 119–127.CrossRefGoogle Scholar
  28. Kopke, D., 1988. The climate of the Eastern Cape. In Bruton, M. N. & F. W. Gess (eds), Towards an Environmental Plan for the Eastern Cape. Rhodes University, Grahamstown.Google Scholar
  29. Kruger, M. & N. A. Strydom, 2011. Plankton dynamics associated with the convergence zone of a shear front in the permanently open Kowie Estuary, South Africa. African Zoology 46: 47–59.CrossRefGoogle Scholar
  30. Kruskal, J. B. & M. Wish, 1978. Multidimensional Scaling. Sage University Paper series on Quantitative Applications in the Social Sciences. Sage Publishers, Beverly Hills and London.Google Scholar
  31. Kühl, M., C. Lassen & N. P. Revsbech, 1997. A simple light meter for measurements of PAR (400–700 nm) with fiber-optic microprobes: application for P vs E0 (PAR) measurements in a microbial mat. Aquatic Microbial Ecology 13: 197–207.CrossRefGoogle Scholar
  32. Lemley, D. A., J. B. Adams & G. C. Bate, 2016. A review of microalgae as indicators in South African estuaries. South African Journal of Botany 107: 12–20.CrossRefGoogle Scholar
  33. Levasseur, M., J.-C. Therriault & C. Legendre, 1984. Hierarchical control of phytoplankton succession by physical factors. Marine Ecology Progress Series 19: 211–222.CrossRefGoogle Scholar
  34. Livingston, R. J., A. K. Prasad, X. Niu & S. E. McGlynn, 2002. Effects of ammonia in pulp mill effluents on estuarine phytoplankton assemblages: field descriptive and experimental results. Aquatic Botany 74: 343–367.CrossRefGoogle Scholar
  35. Longhurst, A., S. Sathyendranath, T. Platt & C. Caverhill, 1995. An estimate of global primary production in the ocean from satellite radiometer data. Journal of Plankton Research 17: 1245–1271.CrossRefGoogle Scholar
  36. Lutjeharms, J. R. E., 2006. The Agulhas Current. Springer-Verlag, Heidelberg.Google Scholar
  37. Margalef, R., 1958. Temporal succession and spatial heterogeneity in phytoplankton. In Buzzati-Traverso, A. A. (ed), Perspective in Marine Biology. University of California Press, Berkeley and Los Angeles.Google Scholar
  38. Nixon, S. W., C. Oviatt, J. Frithsen & B. Sullivan, 1986. Nutrients and the productivity of estuarine and coastal marine ecosystems. Journal of the Limnological Society of South Africa 12: 43–71.CrossRefGoogle Scholar
  39. Nozais, C., R. Perissinotto & S. Mundree, 2001. Annual cycle of microalgal biomass in a South African temporarily-open estuary: nutrient versus light limitation. Marine Ecology Progress Series 223: 39–48.CrossRefGoogle Scholar
  40. Pan, C.-W., Y.-L. Chuang, L.-S. Chou, M.-H. Chen & H.-J. Lin, 2016. Factors governing phytoplankton biomass and production in tropical estuaries of western Taiwan. Continental Shelf Research 118: 88–99.CrossRefGoogle Scholar
  41. Parsons, T. R., Y. Maita & C. M. Lalli, 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York.Google Scholar
  42. Perissinotto, R. & C. Nozais, 2002. Spatio-temporal dynamics of phytoplankton and microphytobenthos in a South African temporarily-open estuary. Estuarine, Coastal and Shelf Science 55: 47–58.CrossRefGoogle Scholar
  43. Perissinotto, R., D. Pillay & G. Bate, 2010. Microalgal biomass in the St. Lucia Estuary during the 2004–2007 drought period. Marine Ecology Progress Series 405: 147–161.CrossRefGoogle Scholar
  44. Roelke, D. L. & S. Spatharis, 2015. Phytoplankton succession in recurrently fluctuating environments. PLoS One 10: e0121392.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Roy, P. S., R. J. Williams, A. R. Jones, I. Yassini, P. J. Gibbs, B. Coates, R. J. West, P. R. Scanes, J. P. Hudson & S. Nichol, 2001. Structure and function of south-east Australian estuaries. Estuarine, Coastal and Shelf Science 53: 351–384.CrossRefGoogle Scholar
  46. Sand-Jensen, K. & J. Borum, 1991. Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries. Aquatic Botany 41: 137–175.CrossRefGoogle Scholar
  47. Sieburth, J. M., V. Smetacek & J. Lenz, 1978. Pelagic ecosystem structure: heterotrophic compartments of the plankton and their relationship to plankton size fractions. Limnology and Oceanography 23: 1256–1263.CrossRefGoogle Scholar
  48. Snow, G. C. & J. B. Adams, 2007. Relating microalgal spatial patterns to flow, mouth and nutrient status in the temporarily open/closed Mngazi estuary, South Africa. Marine and Freshwater Research 58: 1032–1043.CrossRefGoogle Scholar
  49. Snow, G. C. & G. C. Bate, 2009. Response of the microalgae to changes in freshwater inflow in the Berg Estuary, southern Africa. Transactions of the Royal Society of South Africa 64: 189–203.CrossRefGoogle Scholar
  50. SPSS Inc., 2007. SPSS Release 16.0.0 for Windows. Polar Engineering and Consulting. SPSS Inc., Chicago.Google Scholar
  51. Taylor, J. C., W. R. Harding & C. G. M. Archibald, 2005. A Methods Manual for the Collection, Preparation and Analysis of Diatom Samples. Version 1.0. WRC Report No. TT 281/07. Water Research Commission, Pretoria.Google Scholar
  52. Taylor, J. C., W. R. Harding & C. G. M. Archibald, 2007. An illustrated guide to some common diatom species from South Africa. WRC Report TT 282/07. Water Research Commission, Pretoria.Google Scholar
  53. Thomas, C. M., R. Perissinotto & I. Kibirige, 2005. Phytoplankton biomass and size structure in two South African eutrophic, temporarily open/closed estuaries. Estuarine, Coastal and Shelf Science 65: 223–238.CrossRefGoogle Scholar
  54. Tonkin, J. D., M. T. Bogan, N. Bonada, B. Rios-Touma & D. A. Lytle, 2017. Seasonality and predictability shape temporal species diversity. Ecology 98: 1201–1216.CrossRefPubMedGoogle Scholar
  55. Tucker, C. S., S. W. Lloyd & R. L. Busch, 1984. Relationships between phytoplankton periodicity and the concentrations of total and unionized ammonia in channel catfish ponds. Hydrobiologia 111: 75–79.CrossRefGoogle Scholar
  56. van der Molen, J. S. & R. Perissinotto, 2011. Microalgal productivity in an estuarine lake during a drought cycle: The St. Lucia Estuary, South Africa. Estuarine, Coastal and Shelf Science 92: 1–9.CrossRefGoogle Scholar
  57. van Ginkel, C. E., 2012. Algae, phytoplankton and eutrophication research and management in South Africa: past, present and future. African Journal of Aquatic Science 37: 17–25.CrossRefGoogle Scholar
  58. Vinayachandran, P. N. & S. Mathew, 2003. Phytoplankton bloom in the Bay of Bengal during the northeast monsoon and its intensification by cyclones. Geophysical Research Letters 30: 1572.CrossRefGoogle Scholar
  59. Welschmeyer, N. A., 1994. Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnology and Oceanography 39: 1985–1992.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Tatenda Dalu
    • 1
    • 2
  • Mandla L. Magoro
    • 2
    • 3
    • 4
  • Jonathan D. Tonkin
    • 5
  • Lucienne R. D. Human
    • 3
    • 6
  • Renzo Perissinotto
    • 4
  • Shaun H. P. Deyzel
    • 6
    • 7
  • Janine B. Adams
    • 3
  • Alan K. Whitfield
    • 2
  1. 1.Department of Ecology and Resource ManagementUniversity of VendaThohoyandouSouth Africa
  2. 2.South African Institute for Aquatic BiodiversityGrahamstownSouth Africa
  3. 3.Department of Botany, Institute for Coastal and Marine Research (CMR)Nelson Mandela UniversityPort ElizabethSouth Africa
  4. 4.DST/NRF SARChI Shallow Water Ecosystems LaboratoryNelson Mandela UniversityPort ElizabethSouth Africa
  5. 5.Integrative BiologyOregon State UniversityCorvallisUSA
  6. 6.South African Environmental Observation Network (SAEON)Port ElizabethSouth Africa
  7. 7.Department of Zoology, Institute for Coastal and Marine Research (CMR)Nelson Mandela UniversityPort ElizabethSouth Africa

Personalised recommendations