The role of life cycle processes on phytoplankton spring bloom composition: a modelling study applied to the Gulf of Finland
Introduction
In most temperate waters spring blooms are dominated by diatoms (Smayda, 1980, Smayda and Reynolds, 2003). This is not the case in the Baltic Sea, where large (20–30 μm radius/diameter) cold-water dinoflagellates often compete successfully with diatoms (Niemi, 1975, Kononen and Niemi, 1984, Heiskanen, 1993, Heiskanen and Kononen, 1994, Heiskanen, 1998, Kremp and Heiskanen, 1999, Olli and Heiskanen, 1999, Jaanus et al., 2006, Spilling, 2007b). In recent decades, an increasing trend in the spring bloom proportion of cold-water dinoflagellates has been observed in several parts of the Baltic Sea, including the Gulf of Finland (Wasmund and Uhlig, 2003, Alheit et al., 2005, Jaanus et al., 2006, Klais et al., 2011, Wasmund et al., 2011, Klais et al., 2013). The causes behind this trend, however, are unclear.
Generally, dinoflagellates are considered to be less competitive compared to diatoms. Spring bloom dinoflagellates from the Baltic Sea for example have a lower maximum light utilization coefficient (Spilling, 2007b, Spilling and Markager, 2008), a narrower temperature window (Kremp et al., 2005) and a lower maximum growth rate (Spilling, 2007b, Spilling and Markager, 2008) than diatoms. Given these competitive disadvantages, the apparent paradox (low maximum specific growth rate but sudden bloom formation of dinoflagellates) may be related to life cycle aspects (see, e.g., Hense and Burchard, 2010).
Individual life cycle strategies seem to be important in regulating dinoflagellate blooms (Anderson and Rengefors, 2006, Bravo et al., 2010, Kremp, 2013, Wyatt and Zingone, 2014). For example, Biecheleria baltica (sensu Moestrup et al., 2009 = Woloszynskia halophile sensu Kremp et al. (2005)), one of the dominant spring bloom dinoflagellate species in the Gulf of Finland, forms numerous resting cysts at the end of the bloom period (Olli and Trunov, 2010); the accumulation of cysts in the sediment leads to the formation of seed banks. Enhanced encystment and the spreading of cyst beds are assumed to increase the abundance of this species in the water column (Olli and Trunov, 2010, Klais et al., 2011). Kremp et al. (2008) have emphasized that the size of the inoculum regulates bloom formation and the dominance of the cold-water dinoflagellates over diatoms. In their mesocosm experiments, nutrient concentrations and elemental ratios have played a minor role in influencing the competition between dinoflagellates and diatoms.
In general, however, changes in nutrient conditions as well as elemental ratios as a result of eutrophication are often made responsible for ecosystem changes in the Baltic Sea. In particular, high nitrogen and phosphorus loading over decades (see e.g. Elmgren, 2001) but a decrease in the land-sea flux of silica (Humborg et al., 2006) suggest that conditions for diatom growth have deteriorated in the Baltic Sea. However, the silica:nitrogen ratio, specifically in the Gulf of Finland, is quite high (2.0, Papush and Danielsson, 2006) and field studies in the entire Baltic Sea have shown that the spring bloom is limited by nitrogen (Tamminen and Anderson, 2007). Thus, although nutrient concentrations definitely control the total biomass concentrations, it seems unlikely that they can explain the observed long-term trends and neither do the corresponding nutrient ratios.
Other explanations regarding the increasing trend in the spring bloom proportion of dinoflagellates have been put forward, such as decadal climate oscillations (Wasmund et al., 1998, Alheit et al., 2005) or the decrease in ice cover (Klais et al., 2011, Klais et al., 2013). Both seem plausible, as they are consistent with a stronger stratification in winter and spring: since dinoflagellates prefer such stratified conditions, they may have a competitive advantage over diatoms, who do not. The same argument may be used to attribute the trend in species composition to global warming. However, rising temperatures have also more direct effects on growth and life cycle processes of phytoplankton. And some of these effects, e.g., the temperature-dependence of growth, or the life cycle transition regulation and germination control of dinoflagellates (Kremp and Anderson, 2000, Anderson and Rengefors, 2006), may or may not favor dinoflagellate species. In summary, existing observational evidence alone does not easily lead to an explanation of the positive trend in the proportion of dinoflagellates.
Ecosystem models may be a useful tool to address some of the open questions regarding the observed trend. As the inoculum and thus life cycle aspects seem to be important, such an ecosystem model needs to consider life cycle processes of both diatoms and dinoflagellates. So far, there are only few model studies that take these processes into account. Eilertsen and Wyatt (2000) have shown that the consideration of the seed stock better explains spring bloom dynamics in high latitudes. Warns (2013) has coupled a complex dinoflagellate life cycle model (Warns et al., 2013a, Warns et al., 2013b) with a simple diatom life cycle model and found that the alternating patterns between diatoms' and dinoflagellates' dominance can be explained by the abundance of the resting stages and the temperature gradient in spring. Neither of these studies, however, has addressed the observed increasing trend of the spring bloom proportion of dinoflagellates in the Baltic Sea.
By using an ecosystem model that resolves the life cycle of both dinoflagellates and diatoms, we specifically want to understand the underlying mechanisms leading to the increasing trend found in the spring bloom proportion of dinoflagellates in the Gulf of Finland for the period 1981–2010. Our ecosystem model is coupled to a water column model and considers the life cycle processes of three main Baltic Sea phytoplankton groups (diatoms, dinoflagellates and cyanobacteria). We are particularly interested in answering the following questions: (1) is the model able to reproduce the observed trend? If so, (2) what are the underlying mechanisms leading to it?
Section snippets
Observations
We will compare our model results with observations from the Gulf of Finland (longitude 24.8°E, latitude 54.8°N). Specifically, we use the Helsinki Commission (HELCOM) monitoring data for nutrients from the International Council for the Exploration of the Seas (ICES) database (ICES, 2016) and the phytoplankton monitoring datasets which are provided by national monitoring agencies (Klais et al., 2011). Although the phytoplankton data set covers all seasons and includes various taxonomic groups,
Model description
Our model is based on a Baltic Sea ecosystem model, the Ecological ReGional Ocean Model, (ERGOM, Neumann, 2000, Neumann et al., 2002), with an improved description of the phytoplankton groups: we now consider the life cycles of diatoms (Warns, 2013), dinoflagellates (Warns et al., 2013a, Warns et al., 2013b) and cyanobacteria (Hense and Beckmann, 2006, Hense and Burchard, 2010). All other ecosystem variables and processes of ERGOM (related to zooplankton, the three nutrients (nitrate, ammonium
Climatologies
Fig. 2 shows modeled and observed climatological seasonal patterns of sea surface temperature (SST) and surface DIN concentrations for the past three decades. Overall, the climatological seasonal cycles of environmental conditions in the Gulf of Finland are well reproduced. During winter (January–February) the simulated SST is slightly lower, during summer (June–August) somewhat higher than the observed SST (Fig. 2a). The simulated seasonal cycle of DIN concentrations is similar but with a time
Discussion and conclusions
We have investigated the trend in spring bloom composition in the Gulf of Finland, Baltic Sea for the period 1981–2010 by using a coupled water column-ecosystem model which includes the life cycle of three main Baltic Sea phytoplankton groups (diatoms, dinoflagellates and cyanobacteria). In agreement with observations, the model results show an increasing proportion of dinoflagellates in the spring bloom biomass. The altered dominance between diatoms and dinoflagellates is determined by changes
Acknowledgements
We thank two anonymous referees for their valuable comments, which helped to improve the manuscript. We are grateful to Riina Klais for making the observational data of diatoms and dinoflagellates available. We also thank ICES for the HELCOM monitoring data (temperature, salinity and nutrients) and ECMWF for the meteorological forcing data. This research was supported through the Cluster of Excellence “CliSAP” (EXC177), Universität Hamburg, funded through the German Science Foundation (DFG).
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