Estimation of new production in the North Sea: consequences for temporal and spatial variability of phytoplankton

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1 ICES Journal of Marine Science, 55: Article No. jm Estimation of new production in the North Sea: consequences for temporal and spatial variability of phytoplankton Katherine Richardson and Flemming Bo Pedersen Richardson, K., and Bo Pedersen, F Estimation of new production in the North Sea: consequences for temporal and spatial variability of phytoplankton ICES Journal of Marine Science, 55: By coupling knowledge of oceanographic processes and phytoplankton responses to light and nutrient availability, we estimate a total potential new production for the North Sea of approximately t C year 1. In a typical year, about 40% of this production will be associated with the spring bloom in the surface waters of the seasonally stratified central and northern regions. About 40% is predicted to occur in the coastal waters while the remaining new production is predicted to take place in subsurface chlorophyll peaks occurring in association with fronts during summer months. By considering inter-annual variation in heat, wind, and nutrient availability (light and tidal energy input are treated as non-varying from year to year), the inter-annual variability in the new production in different regions is estimated. The analysis indicates that new production in the coastal waters may have increased by about 25% in recent decades International Council for the Exploration of the Sea Key words: fronts, inter-annual variability, new production, North Sea, nutrient availability, total production, seasonal stratification, spring bloom, subsurface chlorophyll peaks. K. Richardson: Department of Marine Ecology, Arrhus University, Finlandsgade 14, DK-8200 Arrhus, Denmark; F. Bo Pedersen: ISVA, Technical University of Denmark, Building 115, DK-2800 Lyngby, Denmark. Correspondence to K. Richardson: tel: ; fax: ; richardson@biology.aau.dk Introduction Examination of temporal trends in marine phytoplankton distribution and activity requires data spanning the time period in question. Given the natural variability expressed by biological systems, long time series are generally needed to identify real changes in plankton abundance. Such data sets are often developed by compiling data collected from different laboratories. The strategy of data collection programmes is usually based on the understanding of phytoplankton ecology at the time the programme was initiated. As our understanding becomes more sophisticated, so do sampling strategies and, therefore, direct comparison of data from different time periods may not be meaningful. It is now clear, for example, that any consideration of the primary production of the North Sea as a whole must consider the production in both surface and subsurface waters (Richardson and Christoffersen, 1991; Nielsen et al., 1993). Richardson et al. (1998) have shown that, at stations in the stratified region of the North Sea, up to 70% of the daily primary production during the summer may occur in subsurface chlorophyll peaks. As sampling at standard depths often misses the existence of narrow subsurface peaks, extreme care must be exercised when comparing primary production measurements made today with our modern understanding of phytoplankton ecology with those made in the 1960s and early 1970s when it was customary to sample at standard depths. The best time series for phytoplankton abundance and activity in the North Sea in terms of sampling frequency are those collected near shore, where there is relatively easy access. However, it is difficult when examining a coastal data set for potential changes in phytoplankton abundance to estimate what effect an identified change may have on primary production in the North Sea as a whole. The studies referred to above indicate that there is a clear coupling between the oceanographic processes occurring in and the phytoplankton ecology of the North Sea. Understanding the mechanisms behind this coupling will provide the possibility to consider the sensitivity of the ecosystem with respect to changes in the parameters controlling the biological oceanography /98/ $30.00/ International Council for the Exploration of the Sea

2 Estimation of new production in the North Sea 575 of the system and to predict the effect that changes in these parameters may have on phytoplankton. These parameters include nutrient input, light, wind, tidal currents, heat fluxes, and freshwater input. The purpose of this study, then, is to synthesize the available information on coupling between phytoplankton and oceanographic processes in order to arrive at a description of the interaction for the North Sea as a whole. We then use this synthesis to give a crude preliminary estimate of the relative importance of different regions to the total primary production of the North Sea. Such a synthesis will provide a useful background for assessing the validity of time series established through data compilation as well as for estimating the basin scale importance of local changes in phytoplankton abundance. Oceanographic processes affecting phytoplankton dynamics Oceanographic processes influence phytoplankton production by controlling the availability of light and nutrients. It is especially in regions where different water masses make contact that new combinations of light and nutrient availability are created. This, of course, explains why biomass accumulations are often encountered in association with fronts where stratified and mixed waters meet. The degree of vertical stratification in the water column is determined by the combined influence of stabilizing and destabilizing forces. The two most important stabilizing processes in the North Sea are the surface heating rate and the input of fresh water via rivers. As a rule, temperature (surface heating) dominates the stability structure in deeper waters, while salinity (river run-off) is a more important controlling factor in the more shallow, near-coast areas. Stability can be quantified as the water column s potential energy and is relatively easy to calculate. In order to break down the stratification, mixing energy must be supplied to the system. The three most important mixing agents in nature are wind, tidal currents, and cooling. Changes in the water column s potential energy can be empirically related to the production of turbulent kinetic energy. During summer, a stratified water column characterizes the central (and deeper) parts of the North Sea. A frontal region will thus be formed separating the offshore stratified waters and the mixed coastal waters. The position of the frontal regions can be predicted by considering the factors controlling stratification. The first study of front positions based on a comparison of field observations and theoretical considerations was produced by Simpson and Hunter (1974), who started with the simplest case and only considered the effect of surface heating and tidal mixing. Their simple stability parameter predicted a tidal excursion of the frontal position between spring and neap tides that was about five times greater than the one actually observed. By taking heat storage into account (Simpson and Bowers, 1981) and by further including wind mixing (Pedersen, 1994), it is now possible to accurately predict frontal movements. Here, we refer to stratified waters as those found on the offshore side of the front, while we refer to coastal waters as those found on the inshore side. Spatial variability in phytoplankton production patterns In stratified waters, new production (sensu Dugdale and Goering, 1967) will take place in surface waters in connection with the spring bloom which occurs immediately after the onset of stratification. During the spring bloom, nutrients mixed into surface waters during winter storms are utilized by phytoplankton. During the following period, little new production will take place in surface waters as few new nutrients are introduced here. Evidence has been emerging in recent years, however, for the occurrence of new production in subsurface phytoplankton peaks in stratified areas during summer months (Nielsen et al., 1993; Richardson et al., 1998). In addition, we predict new production will occur after the spring bloom in coastal waters due to the introduction of new nutrients. The order of magnitude of the new production occurring in association with the spring bloom, i.e., at the time of the transition from the winter (isothermal water column) to summer (stratified) situation, can be estimated. Stratification in the North Sea begins, on average, during May (Pedersen, 1994) and the depth of the early thermocline usually lies at around 30 m (Becker, 1981). The stratified surface layer at this time of the year covers the area from about 1 W 7 E to N. Thus, the volume of the surface layer is approximately m 3. We know that the nutrients in this layer are used up in connection with the spring bloom and that an average winter nitrate concentration in this part of the North Sea is approximately 8 μm (Brockmann and Wegner, 1996). Converting the nitrate concentration in this layer to carbon production using the Redfield ratio (C:N=5.68 by weight) suggests a new production in the order of t C to occur in association with the spring bloom in the stratified region. A similar approach can be used for estimating the magnitude of new primary production taking place in the waters extending from the coast and out to the frontal region, which marks the transition from mixed to stratified waters during the summer months. We define this coastal region as being a belt of approximately km along the coast with an average depth of

3 576 K. Richardson and F. Bo Pedersen 54 N,O E 0 50 km N,2 E x Thermocline 25 y F, min m y F, min y F, max 50 y F, max 75 Front Flamborough Head Front Dogger Bank Figure 1. Cross section of a transect crossing the Dogger Bank and Flamborough Head fronts. Extremes in thermocline position are shown. y F,min =minimal frontal depth; y F,max =maximum frontal depth. Hatched areas indicate volume of water replaced during frontal excursions (see Bo Pedersen, 1994, for a detailed description of the theory used to identify extremes in thermocline position). 20 m. This gives a volume of m 3 for coastal water. We assume a start concentration (pool) of nitrate in this volume of 20 μm, which will give a pool of t nitrogen. We arrive at this value by taking the annual supply of nitrate to this region ( t nitrogen, see below) and assuming an average retention time in the coastal waters of 4 months. Sehested Hansen et al. (1994) reported that the advection of total nitrogen through the English Channel is t per year. We assume that all of this is in an inorganic form that can be used by phytoplankton. North Sea Task Force (1993) reports that riverine and direct input of nitrate accounts for approx t per year. Atmospheric deposition of nitrate into the entire North Sea is estimated to be t. There is little data on the geographic distribution of the atmospheric input. Therefore, we have arbitrarily selected a value of 2 t per year to fall in the coastal region. For the sake of argument, we assume that the entire pool of nitrate in coastal waters at the beginning of the productive season is converted to carbon through photosynthesis. In addition, we assume that 1/2 of the t entering this region per year is available during the productive season. This would allow a new production occurring here of about (from the nitrogen pool) plus t C (from the annual external input of nitrogen) per year. There remains to consider the potential new production occurring in connection with subsurface phytoplankton peaks on the stratified side of the front during summer. This is difficult to estimate as there is no universally accepted description of the oceanographic mechanisms that lead to their formation. Field data (Nielsen et al., 1993; Richardson et al., 1998) clearly show that subsurface chlorophyll peaks are not uniformly distributed over the stratified region. A number of studies have shown that these peaks are most intense near frontal regions (Pingree et al., 1975; Riegman et al., 1990; Creutzberg, 1985; Nielsen et al., 1993; Richardson et al., 1998). Both Nielsen et al. and Richardson et al. argue, on the basis of characteristics of the planktonic food web, that a substantial proportion of the production occurring in these near front subsurface peaks must be new production. Bo Pedersen (1994) has hypothesized a tidal pumping mechanism by which nutrient-rich water could be introduced to the pycnocline layer and which could potentially deliver new nutrients to the bottom of the euphotic zone and, thus, result in new production. While recognizing that this theory has yet to be confirmed through observation, we have elected to use it here to estimate the supply of new nutrients to the pycnocline layer in order to estimate the potential subsurface new production. By applying this theory to the Flamborough Head Dogger Bank transect (Fig. 1), the 2-week tidal pump volumes can be estimated to m 3 per m coastline. This transect is chosen because it traverses two fronts: the Dogger Bank and the Flamborough Head Front. We assume the pump volume calculated for the Dogger Bank front is typical for the fronts occurring on the eastern side of the North Sea and the Flamborough Head volume typical for those on the western side. Thus, we multiply the pump volume calculated for the transect

4 Estimation of new production in the North Sea 577 by 500 km (i.e., the approximate north south length of the North Sea) to arrive at an estimate of m 3 for the volume of water pumped into the thermocline layer per 2-week tidal cycle. Direct measurements of nutrient concentration in the waters bordering the frontal zone throughout the production cycle are not available. However, the theory predicts that the water being pumped into the thermocline layer is a mixture of surface and bottom waters from the stratified side of the front mixed with the more coastal waters during the most recent retreat of the frontal position. Bottom waters in the stratified region of the central North Sea have a nitrate concentration of between about 4 and 6 μm during the summer months (H. Dooley, pers. comm.). We assume, therefore, for the sake of argument, that the water pumped into the thermocline layer has an average NO 3 content of 3 μm and that the thermocline layer has enough light to support phytoplankton photosynthesis. We can then use the Redfield ratio to estimate the order of magnitude for the new production that may be occurring as a result of the tidal excursion of fronts in the North Sea, which amounts to t C during the season (assuming nine 2-week tidal cycles in a growth season). Our rough estimate of the total annual new production occurring in the North Sea is thus t C per year (corresponding to about 40 g m 2 y 1 ). In a typical year, approximately 40% of this production would occur in association with the spring bloom in the stratified surface waters. About 40% will occur in coastal waters during the entire production period and the remainder will occur in subsurface peaks created by frontal excursions. Temporal variability in phytoplankton production patterns Temporal variability in the production of the regions distinguished can be addressed at both the decadal and the inter-annual level. In our proposed scenario for primary production in the North Sea, new production is controlled by physical processes that allow its development in regions with both sufficient light and nutrients. These processes encompass heat input, freshwater input, wind, tidal currents, nutrient input, and light input. This study considers only the effect on new production of inter-annual and decadal variability in heat, wind, and nutrient input. The upper limit for inter-annual variability in the magnitude of new production occurring in association with the spring bloom is estimated on the basis of temperature and wind data collected in May, 1992, a year and month characterized by particularly low wind activity (Fig. 2a) and high heat input. A thermocline became established at 45 m depth (approximately the depth of the photic zone) on 12 13th May (Fig. 2b). From this time onwards, the surface layer is separated from the bottom layer. Several more thermoclines were developed in the succeeding period. As the primary thermocline occurs at 45 m, we argue that all of the nutrients above this depth will be used during the transition from the isothermal to the stratified situation. Thus, the new production during the spring bloom of 1992 might have been about 50% more than during a typical year when the first thermocline develops at 30 m. At the other extreme, the minimum depth of thermocline development in the North Sea appears to be about 18 m (Becker, 1981). In such years, the spring bloom production would only constitute about 60% of the one in a typical year. Thus, we estimate a range of between about 4 and t C fixed per year in association with the spring bloom in the stratified surface waters of the North Sea. Inter-annual variability in the potential new production in the isothermal coastal waters will largely be controlled by changes in riverine and air-borne nutrient input to this region and changes in inflow through the English Channel. Based on inter-annual fluctuations in run-off to the Kattegat in the 1980s, we estimate that the order of magnitude of the inter-annual variability in riverine nutrient input to the North Sea is 15%. We have no data concerning advection of nutrients through the English Channel but, for the sake of argument, assume that it does not vary dramatically from year to year. The inter-annual variation in nutrient input to the coastal regions can be directly converted to potential inter-annual variation in new primary production. Again using the Bo Pedersen (1994) arguments, it is possible to crudely estimate the inter-annual variability in the volume of water that is pumped into the thermocline layer (and the associated potential for new production in this layer) at fronts. As above, we assume that the processes along the Flamborough Head/Dogger Bank transect are typical for the North Sea. The two most important factors contributing to inter-annual variability in the position of fronts are heat input (Q s ) and wind energy (wind 3 ). Both Q s and wind 3 can be expected to vary within a range of 15% from year to year. A percentage change in Q s will be directly but inversely related to a percentage change in water entering the thermocline layer. As an example, a 15% increase in heat input to the system will result in a 15% decrease in the water volume pumped into the thermocline layer. A 15% increase in wind energy will, on the other hand, result in an increase of 11% in the volume. (There is not direct proportionality between changes in wind energy and the volume of water pumped because tidal energy is also a destabilizing force and it remains unchanged). While these two processes affect the pumped volume in opposite directions, they are unlikely

5 578 K. Richardson and F. Bo Pedersen (a) 3000 Wind energy [(ms 1 ) 3 ] Mean May April 1992 May 1992 (b) 0 5 Temperature ( C) C May C 12.4 m 22.5 m Depth (m) C May 45 m C April 70 m Figure 2. (b) Temperature profile recorded on a cruise with RV Dana in the stratified waters north of Dogger Bank ( N; E, 24 May 1992) with indication of the dates on which the individual thermoclines presumably became established; (a) recorded wind energy (wind 3 ) during April/May Note that establishment of the primary and secondary thermoclines can be related to periods with low wind energy input. to cancel each other out, as high wind energy input is usually associated with a low Q s and vice versa. Hence, the combined effects of the inter-annual variability in heat input and in wind energy is estimated to give a 20% variation in the water volume entering the thermocline layer. Decadal variability in the potential new production associated with the regions distinguished can be estimated by considering the influence of decadal changes in the physical parameters controlling the nutrient inputs. With the exception of riverine inputs, we know of no convincing demonstration of long-term trends in these control parameters. Some workers have demonstrated an increase in average annual wind energy input over the North Sea (e.g., Svendsen, 1991). However, Jacobsen (1994) has shown that this increase has occurred during the autumn and winter periods. No increase in average wind energy input could be identified during the spring and summer periods when most phytoplankton production occurs.

6 Estimation of new production in the North Sea 579 Table 1. Estimated new production and associated inter-annual and decadal variation for various regions in the North Sea. Region Sehested Hansen et al. (1994) have estimated that riverine input of N to the North Sea has doubled during the last 25 years. Riverine and atmospheric nutrient input accounts, today, for about 1/2 of the annual nitrogen input to the coastal region, and thus fuels 1/2 of the potential new production. We argue, then, that the doubling of riverine nitrogen input will have resulted in a ca. 25% increase in new primary production in coastal water during recent decades. Discussion New production (t) Inter-annual variability Decadal variability Coastal % +25% Frontal* % (+?) Stratified** % (0) Total % +10% *Subsurface peaks. **Spring bloom in surface waters. Our conclusions with respect to the potential magnitude of new primary production occurring in various regions of the North Sea are summarized in Table 1. Here, it is important to bear in mind that it is new production (sensu Dugdale and Goering, 1967) or the potential for the creation of new organic material from the input of nitrogen to the system that we are considering. Thus, our estimates cannot be directly compared to measurements of total primary production which include regenerated production (originating from the re-use of nitrogen within the system; cf. Dugdale and Goering, 1967). We have not been able to locate other published estimates of annual new production in the North Sea as a whole. However, measurements of sedimentation rates and organic content in sediment have yielded estimates of new production in the more eutrophied Kattegat of about 60 g C m 2 year 1 (Olesen and Lundsgaard, 1995; Jørgensen and Revsbech, 1989). Thus, our North Sea estimate of about 40 g C m 2 would appear to be of a reasonable order of magnitude. Between about 10 and 20% (depending on wind and weather conditions) of this new production is predicted to occur in association with subsurface chlorophyll peaks located near the frontal zone separating coastal waters from the seasonally stratified offshore waters. This production takes place over the entire summer at predictable sites and may be particularly important for the transfer of energy in the pelagic food web during this time of year (Richardson et al., 1998). The subsurface phytoplankton biomass accumulations will not be detected by currently employed air-borne remote sensing methods. Thus, the existence of these productive sub-surface peaks potentially presents a significant source of error in estimates of primary production made using data collected via, for example, satellite sensors. Hill et al. (1994) suggested that the Flamborough Head front may act as a barrier preventing contaminants in coastal waters from entering the more open regions of the North Sea. However, if Pedersen s (1994) prediction of a flow of water (originating, in part, from the coastal waters) into the thermocline layer of the stratified region in association with frontal excursions is correct, then these fronts would actually contribute actively to the transfer of river-borne contaminants to the central North Sea. Similarly, we suggest that the observed increase in nutrient input over time to coastal regions may have increased the potential new production occurring in subsurface chlorophyll peaks in the stratified waters. Analyses such as presented here are important when considering temporal trends in phytoplankton activity for at least two reasons. Firstly, they enable us to make predictions about inter-annual variability based on changes in climatic and anthropogenic influences on the marine environment. Such knowledge can then be used to estimate the length of data series required to identify trends in plankton activity. Secondly, they emphasize the importance of considering the strategy used for data collection when assembling data for the analysis of temporal changes in biological parameters. Strategies for data collection are usually designed based on the currently accepted understanding of how the ecosystem functions. Understanding of ecosystem function changes over time. Thus, data collected in different time periods may not be directly comparable. For example, it has earlier been assumed that all primary production is restricted to the surface layer. Thus, no measurements were made below the thermocline. However, recent studies have shown that subsurface production during summer months is actually higher than production at the surface in some areas (Richardson et al., 1998; Nielsen et al., 1993). Here, we estimate that approximately 20% of annual new production occurs in subsurface chlorophyll peaks. Comparing water column primary production estimates made prior to the discovery of subsurface production with those made after would lead to the (probably false) conclusion that primary production rates have increased in recent years in offshore regions of the North Sea. References Becker, G. A Beiträge zur Hydrographie und Wärmebalanz der Nordsee. Deutsche Hydrographische Zeitschrift, 5:

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