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Spatial and temporal trends in order richness of marine phytoplankton as a tracer for the exchange zone between coastal and open waters

Published online by Cambridge University Press:  20 October 2016

A.S. Jung*
Affiliation:
Royal Netherlands Institute for Sea Research (NIOZ), Department of Coastal Systems, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, the Netherlands
R. Bijkerk
Affiliation:
Koeman en Bijkerk, P.O. Box 111, 9750 AC Haren, the Netherlands
H.W. Van Der Veer
Affiliation:
Royal Netherlands Institute for Sea Research (NIOZ), Department of Coastal Systems, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, the Netherlands
C.J.M. Philippart
Affiliation:
Royal Netherlands Institute for Sea Research (NIOZ), Department of Coastal Systems, and Utrecht University, P.O. Box 59, 1790 AB Den Burg, the Netherlands Department of Physical Geography, University of Utrecht, P.O. Box 80.115, 3508 TC Utrecht, the Netherlands
*
Correspondence should be addressed to: A.S. Jung, Department of Coastal Systems and Utrecht University, Royal Netherlands Institute for Sea Research (NIOZ), P.O. Box 59, 1790 AB Den Burg, The Netherlands Email: [email protected]

Abstract

Quantifying exchange of particulate matter between coastal and open waters is an important and often unresolved issue. Here, we apply phytoplankton order richness as an innovative marine tracer to identify the geographic position of a coastal exchange zone in the SE North Sea, including its variability in time and space. Previous observations on dynamics of suspended particulate matter accumulation resulted in a hypothesized boundary between coastal waters (including the Wadden Sea) and open North Sea waters, the so-called ‘line-of-no-return’. Our study along two transects (Terschelling, Noordwijk) in the Dutch coastal zone showed seasonality patterns in phytoplankton order richness, both for diatoms and flagellates. The coastal Wadden Sea was found to be clearly different from the open North Sea, implying that seasonality in Wadden Sea phytoplankton is at least partly driven by local environmental conditions. Seasonality in flagellates was found to be more uniform than seasonality in diatoms. Stations in the coastal North Sea to a distance of 10 km (Terschelling) to 20 km (Noordwijk) from the shore appeared to be at the inside of the ‘line-of-no-return’. Our findings indicate that this approach is a useful aid in exploring mixing of particulate matter between coastal and open waters and to study the responses of phytoplankton communities to environmental drivers.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

REFERENCES

Alvarez-Fernandez, S., Lindeboom, H.J. and Meesters, H.W.G. (2012) Temporal changes in plankton of the North Sea: community shifts and environmental drivers. Marine Ecology Progress Series 462, 2138.CrossRefGoogle Scholar
Armbrust, E.V. (2009) The life of diatoms in the world's oceans. Nature 459, 185192.CrossRefGoogle ScholarPubMed
Balmford, A., Green, M.J.B. and Murray, M.G. (1996) Using higher-taxon richness as a surrogate for species richness: I. Regional tests. Proceedings of the Royal Society of London B: Biological Sciences 263, 12671274.Google Scholar
Baretta-Bekker, J.G., Baretta, J.W., Latuhihin, M.J., Desmit, X. and Prins, T.C. (2009) Description of the long-term (1991–2005) temporal and spatial distribution of phytoplankton carbon biomass in the Dutch North Sea. Journal of Sea Research 61, 5059.CrossRefGoogle Scholar
Beukema, J.J. and Cadée, G.C. (1986) Zoobenthos responses to eutrophication of the Dutch Wadden Sea. Ophelia 26, 5564.CrossRefGoogle Scholar
Beukema, J.J., Honkoop, P.J.C. and Dekker, R. (1998) Recruitment in Macoma balthica after mild and cold winters and its possible control by egg production and shrimp predation. In Baden, S., Phil, L., Rosenberg, R., Strömberg, J.-O., Svane, I. an Tiselius, P. (eds) Recruitment, colonization and physical-chemical forcing in marine biological systems. Volume 132 of developments in hydrobiology. Dordrecht: Springer, pp. 2334.Google Scholar
Burnham, K.P. and Anderson, D.R. (2002) Model selection and multimodel inference: a practical information-theoretic approach. New York, NY: Springer Science & Business Media.Google Scholar
Carneiro, F.M., Nabout, J.C., Galli Vieira, L.C., Lodi, S. and Bini, L.M. (2013) Higher taxa predict plankton beta-diversity patterns across an eutrophication gradient. Natureza & Conservaçao 11, 4347.CrossRefGoogle Scholar
Carstensen, J., Klais, R. and Cloern, J.E. (2015) Phytoplankton blooms in estuarine and coastal waters: seasonal patterns and key species. Estuarine, Coastal and Shelf Science 162, 98109.CrossRefGoogle Scholar
Cloern, J.E. and Dufford, R. (2005) Phytoplankton community ecology: principles applied in San Francisco Bay. Marine Ecology Progress Series 285, 1128.CrossRefGoogle Scholar
Cloern, J.E. and Jassby, A.D. (2008) Complex seasonal patterns of primary producers at the land–sea interface. Ecology Letters 11, 12941303.CrossRefGoogle ScholarPubMed
Cloern, J.E. and Jassby, A.D. (2010) Patterns and scales of phytoplankton variability in estuarine–coastal ecosystems. Estuaries and Coasts 33, 230241.CrossRefGoogle Scholar
de Jonge, V.N. (1990) Response of the Dutch Wadden Sea ecosystem to phosphorus discharges from the River Rhine. In McLusky, D.S., de Jonge, V.N. and Pomfret, J. (eds) North Sea – estuaries interactions. Dordrecht: Springer, pp. 4962.CrossRefGoogle Scholar
de Jonge, V.N. and de Jong, D.J. (2002) ‘Global change’ impact of inter-annual variation in water discharge as a driving factor to dredging and spoil disposal in the river Rhine system and of turbidity in the Wadden Sea. Estuarine, Coastal and Shelf Science 55, 969991.CrossRefGoogle Scholar
de Jonge, V.N., Essink, K. and Boddeke, R. (1993) The Dutch Wadden Sea: a changed ecosystem. In Best, E.P.H. and Bakker, J.P. (eds) Netherlands-Wetlands. Dordrecht: Springer, pp. 4571.CrossRefGoogle Scholar
de Vries, I., Duin, R.N.M., Peeters, J.C.H., Los, F.J., Bokhorst, M. and Laane, R.W.P.M. (1998) Patterns and trends in nutrients and phytoplankton in Dutch coastal waters: comparison of time-series analysis, ecological model simulation, and mesocosm experiments. ICES Journal of Marine Science 55, 620634.CrossRefGoogle Scholar
Field, C.B., Behrenfeld, M.J., Randerson, J.T. and Falkowski, P. (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237240.CrossRefGoogle ScholarPubMed
Finkel, Z.V., Beardall, J., Flynn, K.J., Quigg, A., Rees, T.A.V. and Raven, J.A. (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32, 119137.CrossRefGoogle Scholar
Gallego, I., Davidson, T.A., Jeppesen, E., Pérez-Martinez, C., Sánchez-Castillo, P., Juan, M., Fuentes-Rodríguez, F., León, D., Peñalver, P., Toja, J. and Casas, J.J. (2012) Taxonomic or ecological approaches? Searching for phytoplankton surrogates in the determination of richness and assemblage composition in ponds. Ecological Indicators 18, 575585.CrossRefGoogle Scholar
Gaston, K.J. and Williams, P.H. (1993) Mapping the world's species-the higher taxon approach. Biodiversity Letters 1, 28.CrossRefGoogle Scholar
Gotelli, N.J. and Colwell, R.K. (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4, 379391.CrossRefGoogle Scholar
Guiry, M.D. (2012) How many species of algae are there? Journal of Phycology 48, 10571063.CrossRefGoogle Scholar
Heino, J. and Soininen, J. (2007) Are higher taxa adequate surrogates for species-level assemblage patterns and species richness in stream organisms? Biological Conservation 137, 7889.CrossRefGoogle Scholar
Hutchinson, G.E. (1961) The paradox of the plankton. American Naturalist 95, 137145.CrossRefGoogle Scholar
Koeman, R.P.T., Brochard, C.J.E., Loonen, M.J.J.E. and Fockens, K. (2005) Geannoteerde soortenlijst biomonitoring fytoplankton Nederlandse zoute wateren 1990–2004. Rapport 2005-023. Haren: Bureau Koeman en Bijkerk.Google Scholar
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A., Hooper, D.U., Huston, M.A., Raffaelli, D., Schmid, B., Tilman, D. and Wardle, D.A. (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294, 804808.CrossRefGoogle ScholarPubMed
Machado, K.B., Borges, P.P., Carneiro, F.M., de Santana, J.F., Vieira, L.C.G., de Moraes Huszar, V.L. and Nabout, J.C. (2015) Using lower taxonomic resolution and ecological approaches as a surrogate for plankton species. Hydrobiologia 743, 255267.CrossRefGoogle Scholar
Mallin, M.A., Paerl, H.W. and Rudek, J. (1991) Seasonal phytoplankton composition, productivity and biomass in the Neuse River estuary, North Carolina. Estuarine, Coastal and Shelf Science 32, 609623.CrossRefGoogle Scholar
Mueller, M., Pander, J. and Geist, J. (2013) Taxonomic sufficiency in freshwater ecosystems: effects of taxonomic resolution, functional traits, and data transformation. Freshwater Science 32, 762778.CrossRefGoogle Scholar
Naeem, S. (2009) Biodiversity, ecosystem functioning, and human wellbeing: an ecological and economic perspective. Oxford: Oxford University Press.CrossRefGoogle Scholar
Naeem, S., Thompson, L.J., Lawler, S.P., Lawton, J.H. and Woodfin, R.M. (1994) Declining biodiversity can alter the performance of ecosystems. Nature 368, 734737.CrossRefGoogle Scholar
Olli, K., Ptacnik, R., Andersen, T., Trikk, O., Klais, R., Lehtinen, S. and Tamminen, T. (2014) Against the tide: recent diversity increase enhances resource use in a coastal ecosystem. Limnology and Oceanography 59, 267274.CrossRefGoogle Scholar
Olli, K., Trikk, O., Klais, R., Ptacnik, R., Andersen, T., Lehtinen, S. and Tamminen, T. (2013) Harmonizing large data sets reveals novel patterns in the Baltic Sea phytoplankton community structure. Marine Ecology Progress Series 474, 5366.CrossRefGoogle Scholar
Otto, L., Zimmerman, J.T.F., Furnes, G.K., Mork, M., Saetre, R. and Becker, G. (1990) Review of the physical oceanography of the North Sea. Netherlands Journal of Sea Research 26, 161238.CrossRefGoogle Scholar
Passy, S.I. and Legendre, P. (2006) Power law relationships among hierarchical taxonomic categories in algae reveal a new paradox of the plankton. Global Ecology and Biogeography 15, 528535.CrossRefGoogle Scholar
Pebesma, E.J. (2004) Multivariable geostatistics in S: the gstat package. Computers and Geosciences 30, 683691.CrossRefGoogle Scholar
Philippart, C.J.M., Beukema, J.J., Cadée, G.C., Dekker, R., Goedhart, P.W., van Iperen, J.M., Leopold, M.F. and Herman, P.M.J. (2007) Impacts of nutrient reduction on coastal communities. Ecosystems 10, 95118.CrossRefGoogle Scholar
Philippart, C.J.M., Cadée, G.C., van Raaphorst, W. and Riegman, R. (2000) Long–term phytoplankton–nutrient interactions in a shallow coastal sea: algal community structure, nutrient budgets, and denitrification potential. Limnology and Oceanography 45, 131144.CrossRefGoogle Scholar
Philippart, M. (1988) Tijdschalen in de Waddenzee (Time scales in the Wadden Sea). Utrecht: Institute for Meteorology and Oceanography (IMOU), State University Utrecht, pp. 151.Google Scholar
Pinckney, J.L., Paerl, H.W., Tester, P. and Richardson, T.L. (2001) The role of nutrient loading and eutrophication in estuarine ecology. Environmental Health Perspectives 109(Suppl. 5), 699.Google ScholarPubMed
Postma, H. (1961) Transport and accumulation of suspended matter in the Dutch Wadden Sea. Netherlands Journal of Sea Research 1, 148190.CrossRefGoogle Scholar
Postma, H. (1981) Exchange of materials between the North Sea and the Wadden Sea. Marine Geology 40, 199213.CrossRefGoogle Scholar
Postma, H. (1982) Hydrography of the Wadden Sea: movements and properties of water and particulate matter: final report on ‘Hydrography’ of the Wadden Sea Working Group. Rotterdam: A. A. Balkema.Google Scholar
Postma, H. (1984) Introduction to the symposium on organic matter in the Wadden Sea. Netherlands Institute for Sea Research Publication Series 10, 1522.Google Scholar
Prins, T.C., Desmit, X. and Baretta-Bekker, J.G. (2012) Phytoplankton composition in Dutch coastal waters responds to changes in riverine nutrient loads. Journal of Sea Research 73, 4962.CrossRefGoogle Scholar
Ptacnik, R., Solimini, A.G., Andersen, T., Tamminen, T., Brettum, P., Lepistö, L., Willén, E. and Rekolainen, S. (2008) Diversity predicts stability and resource use efficiency in natural phytoplankton communities. Proceedings of the National Academy of Sciences USA 105, 51345138.CrossRefGoogle ScholarPubMed
Rue, H., Martino, S. and Chopin, N. (2009) Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 71, 319392.CrossRefGoogle Scholar
Rue, H., Martino, S., Lindgren, F., Simpson, D., Riebler, A. and Krainski, E.T. (2015) INLA: Functions which allow to perform full Bayesian analysis of latent Gaussian models using Integrated Nested Laplace Approximation R package. www.r-inla.org.Google Scholar
Ruppert, D., Wand, M.P. and Carroll, R.J. (2003) Semiparametric regression. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Tett, P., Gowen, R., Grantham, B., Jones, K. and Miller, B.S. (1986) The phytoplankton ecology of the Firth of Clyde sea-lochs Striven and Fyne. Proceedings of the Royal Society of Edinburgh. Section B. Biological Sciences 90, 223238.CrossRefGoogle Scholar
van Beusekom, J.E.E., Brockmann, U.H., Hesse, K.J., Hickel, W., Poremba, K. and Tillmann, U. (1999) The importance of sediments in the transformation and turnover of nutrients and organic matter in the Wadden Sea and German Bight. Deutsche Hydrografische Zeitschrift 51, 245266.CrossRefGoogle Scholar
van Beusekom, J.E.E., Buschbaum, C. and Reise, K. (2012) Wadden Sea tidal basins and the mediating role of the North Sea in ecological processes: scaling up of management? Ocean and Coastal Management 68, 6978.CrossRefGoogle Scholar
van Beusekom, J.E.E. and De Jonge, V.N. (2002) Long-term changes in Wadden Sea nutrient cycles: importance of organic matter import from the North Sea. Hydrobiologia 475, 185194.CrossRefGoogle Scholar
van Raaphorst, W. and de Jonge, V.N. (2004) Reconstruction of the total N and P inputs from the IJsselmeer into the western Wadden Sea between 1935–1998. Journal of Sea Research 51, 109131.CrossRefGoogle Scholar
van Raaphorst, W., Philippart, C.J.M., Smit, J.P.C., Dijkstra, F.J. and Malschaert, J.F.P. (1998) Distribution of suspended particulate matter in the North Sea as inferred from NOAA/AVHRR reflectance images and in situ observations. Journal of Sea Research 39, 197215.CrossRefGoogle Scholar
van Raaphorst, W. and van der Veer, H.W. (1990) The phosphorus budget of the Marsdiep tidal basin (Dutch Wadden Sea) in the period 1950–1985: importance of the exchange with the North Sea. Hydrobiologia 195, 2138.CrossRefGoogle Scholar
Verwey, J. (1954) On the ecology of distribution of cockle and mussel in the Dutch Waddensea, their role in sedimentation and the source of their food supply. Archives Neerlandaises de Zoologie 10, 171239.CrossRefGoogle Scholar
Visser, M., De Ruijter, W.P.M. and Postma, L. (1991) The distribution of suspended matter in the Dutch coastal zone. Netherlands Journal of Sea Research 27, 127143.CrossRefGoogle Scholar
Wand, M.P. and Ormerod, J.T. (2008) On semiparametric regression with O'Sullivan penalized splines. Australian and New Zealand Journal of Statistics 50, 179198.CrossRefGoogle Scholar
Winder, M. and Cloern, J.E. (2010) The annual cycles of phytoplankton biomass. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 32153226.CrossRefGoogle ScholarPubMed
Wolff, W.J. (1983) Ecology of the Wadden Sea. Rotterdam: A. A. Balkema.Google Scholar
Wood, S. (2006) Generalized additive models: an introduction with R. Boca Raton, FL: Chapman & Hall/CRC Press.CrossRefGoogle Scholar
WoRMS Editorial Board (2015) World Register of Marine Species (WoRMS). http://www.marinespecies.org (accessed 10.6.2014 and 7.8.2015).Google Scholar
Zijlstra, J.J. (1972) On the importance of the Wadden Sea as a nursery area in relation to the conservation of the southern North Sea fishery resources. Symposium Zoological Society London 29, 233258.Google Scholar
Zimmerman, J.T.F. and Rommets, J.W. (1974) Natural fluorescence as a tracer in the Dutch Wadden Sea and the adjacent North Sea. Netherlands Journal of Sea Research 8, 117125.CrossRefGoogle Scholar
Zingone, A., Harrison, P.J., Kraberg, A., Lehtinen, S., McQuatters-Gollop, A., O'Brien, T., Sun, J. and Jakobsen, H.H. (2015) Increasing the quality, comparability and accessibility of phytoplankton species composition time-series data. Estuarine, Coastal and Shelf Science 162, 151160.CrossRefGoogle Scholar
Zuur, A.F., Hilbe, J. and Ieno, E.N. (2013) A beginner's guide to GLM and GLMM with R: a frequentist and Bayesian perspective for ecologists. Newburgh: Highland Statistics.Google Scholar
Zuur, A.F., Ieno, E.N. and Elphick, C.S. (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 314.CrossRefGoogle Scholar
Zuur, A.F., Saveliev, A.A. and Ieno, E.N. (2014) A beginner's guide to generalised additive mixed models with R. Newburgh: Highland Statistics.Google Scholar
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