primary production enhancement by artificial upwelling in a … · 2004 and 2005. pumping 2 m3...

MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 352: 39–52, 2007doi: 10.3354/meps07139

Published December 20

INTRODUCTION

Physical processes regulating the vertical structureof the ocean determine marine productivity, as exem-plified by the importance of coastal upwelling systemsin global fisheries (Ryther 1969). In many coastalwaters primary production rates benefit from up-welling of deep water. In this process surface watersare displaced offshore by a one-sided horizontal diver-gence caused by surface Ekman transport and arereplaced by nutrient-rich deep water (Smith et al.1983). The upwelling circulation operates on a widerange of time scales, which include short (hours), inter-mediate (days) and long (seasonal and inter-annual)scales. The large-scale coastal upwelling regions areamong the most productive in the world, with annualprimary production rates of more than 700 g C m–2 yr–1

(Mann & Lazier 1996). These systems favour growth ofdiatoms. Coastal upwelling also supports some of themost productive and successful mussel farming areas

(Pitcher & Calder 1998, Figueiras et al. 2000). Typicalannual primary production rates in Norwegian fjordsand coastal waters are 110 to 140 g C m–2 yr–1 (Eilert-sen & Taasen 1984, Erga & Heimdal 1984, Erga 1989b,Erga et al. 2005), where about 60% takes place afterthe spring bloom during March and April.

In summer fjords are stratified primarily as a result offreshwater runoff and calm wind conditions thatrestrict vertical mixing of nutrients into the euphoticlayer (Aure et al. 1996, Asplin et al. 1999). Nutrientsderived from freshwater runoff, or intermediate waterinflow from the outer fjord or coastal waters, are gener-ally less important than the vertical nutrient flux(Aksnes et al. 1989). Consequently, the euphotic zoneis nutrient-depleted during summer and the primaryproduction rates, which are mainly based on nutrientsregenerated in the water column (Skjoldal et al. 2004),are typically reduced to one-third of spring bloom lev-els (Erga et al. 2005). Primary production rate basedupon new nutrients (e.g. an upward nutrient flux from

© Inter-Research 2007 · www.int-res.com*Email: [email protected]

Primary production enhancement by artificialupwelling in a western Norwegian fjord

Jan Aure1, Øivind Strand1, Svein Rune Erga2, Tore Strohmeier1

1Institute of Marine Research, Nordnesgaten 50, 5817 Bergen, Norway2Department of Biology, University of Bergen, Jahnebakken 5, 5020 Bergen, Norway

ABSTRACT: To enhance primary production rate for shellfish cultivation in fjords, a large-scale arti-ficial upwelling experiment was carried out in a western Norwegian fjord during the summers of2004 and 2005. Pumping 2 m3 s–1 brackish surface water to a depth of 30 m created an artificialupwelling of nutrient-rich deeper water. The entrainment of deeper water into the buoyant brackishplume resulted in a transport of about 450 kg d–1 nitrate, 760 kg d–1 silicate and 75 kg d–1 phosphateto an intrusion depth of 8 to 10 m. The artificial upwelling approximately tripled mean chlorophyll a(chl a) concentration and related primary production rate during the summer within an influence areaof 10 km2 near the head of the fjord. The size of the area of influence and the relative increase of thealgae biomass within it depend on both the water exchange and the photosynthetic effectiveness.The relatively high silicate content of the deeper water stimulated diatom growth inside the areainfluenced by the artificial upwelling. A higher stable level of phytoplankton biomass, dominated bynontoxic species, would probably increase the carrying capacity of seston-feeding shellfish and couldform the basis of more predictable mussel cultivation in fjords.

KEY WORDS: Artificial upwelling · Phytoplankton biomass · Primary production rate · Fjord · Mussel culture

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Mar Ecol Prog Ser 352: 39–52, 2007

deeper waters or supported by drainage from the land)is called ‘new production’ and primary production ratebased upon regenerated nutrients in the upper mixedlayer is called ‘regenerated production’ (Dugdale &Goering 1967, Paasche 1988). Total production is thesum of new production and regenerated production.Wassmann (1990) found that total production wasabout 2.5 times as high as new production in southNorwegian coastal and fjord waters. For the summerupwelling events on the Iberian shelf, northwestSpain, a mean R-value of 2.8 was found (Joint et al.2002).

The Norwegian research programme MARICULT(1996 to 2000) aimed to provide a basis for the evalua-tion of environmental constraints and the potential forgreater supplies of food, raw materials and energyfrom the ocean (Olsen 2002). One of the research top-ics in this programme was enhancement of the produc-tion potential in fjords by the creation of artificialupwelling systems. There are a number of simulated orsmall-scale enrichment experiments using deep water,and it has been proposed to use artificial upwelling inenclosed fjord areas to develop safe production oftoxin-free, high-quality shellfish (Aksnes et al. 1985,Berntsen et al. 2002, Olsen 2002). The possibility ofmoving shellfish into such areas for quality enhance-ment (increased meat content) and toxicity treatmenthas also been considered. To the best of our knowl-edge, the first full-scale experiment on artificialupwelling in coastal waters was carried out in Japan,where concrete panels were installed on the sea bot-tom to divert deep water (40 to 50 m) into the euphoticzone of the water column (Morikawa 2001). A signifi-cant enhancement of phytoplankton and zooplanktonproduction was obtained.

On the basis of the results from observations andmodels simulating upwelling scenarios (Aure et al.2000, Berntsen et al. 2002, McClimans et al. 2002), theMARICULT programme recommended further work tovalidate these results at a fjord-scale testing site todetermine the potential of artificial upwelling ofdeeper nutrient-rich seawater in mariculture applica-tions. Using a numerical buoyant flume model and lab-oratory simulations, McClimans et al. (2002) demon-strated the effectiveness of a submerged discharge offreshwater to force vertical transport of nutrient-richdeep water to the euphotic zone in fjords. Berntsen etal. (2002) employed a coupled physical–chemical–bio-logical model to study primary production rate in anidealized 60 km long, 4 km wide fjord subjected to var-ious submerged freshwater discharge scenarios. Theyconcluded that primary production rate could beenhanced by a factor of 3. Due to the higher silicatecontent of the deeper water, the artificial upwellingtends to stimulate diatom more than flagellate growth

(Egge & Aksnes 1992), thereby reducing the problemin fjords of diarrhetic shellfish toxin (DST) caused byDinophysis spp. (Aune et al. 1996). In view of theseresults the inner part of Lysefjord in western Norwaywas selected to be suitable for a large scale experi-ment, since stratification persists throughout the sum-mer and early autumn months. Conditions there pro-vide sufficient quantities of brackish surface water,easily accessible nutrient-rich deeper water and lim-ited water exchange with the open fjord system. Wepresent the results of our first attempt to perform alarge- scale experiment aimed to determine the poten-tial impacts of artificial upwelling on phytoplanktonbiomass, production and composition.

MATERIALS AND METHODS

Study site. The Lysefjord is located on the southwestcoast of Norway (59° 0’ N, 6° 16’ E) (Fig. 1). The fjord isapproximately 40 km long and 0.5 to 2 km wide. Thesill depth is 14 m, maximum depth is 460 m and thesurface area is 44 km2. The mean tidal range is 0.4 mand the freshwater supply to the Lysefjord variesbetween 40 and 90 m3 s–1, with the highest dischargesoccurring in May. Since hydropower plants becameoperational in 1935 and 1952, the mean freshwaterinput to the fjord during April through September hasdecreased by 30 to 40%.

Forced upwelling. The artificial upwelling system ismounted on a moored platform located outside thefreshwater discharge of a hydropower plant near thehead of the Lysefjord (Fig. 1). Brackish water, takenfrom depths of between 0 and 3 m, is forced downthrough a vertically mounted pipe by an electricalpump (ITT Flygt pump) (Fig. 2). The diameter of thepipe is 1.25 m and the pump power output of 60 kWproduces a flow of about 2 m3 s–1 from the outlet at30 m depth. Due to the buoyancy of the submergedbrackish water it rises to the surface and mixes withthe more saline and nutrient rich deeper water. Theequilibrium depth (Zo) is defined as the depth at whichthe density of the rising plume is equal to the density ofthe ambient water, and the intrusion depth (Zi) isexpected to be a few metres above Zo (McClimans etal. 2002). The mean mixing rate of the brackish waterand seawater and related intrusion level was estimatedby adding fluorescein dye to the submerged brackishwater.

Observations. Four sampling stations were set upwithin the main observation area Ao (Stns 11, 16, 17and 01) (Fig. 1). The surface area and average width ofthe fjord inside Ao are 10 km2 and 1 km, respectively.Outside this area we set up Stns 18, 02, 14 in the cen-tral and outer part of the fjord and Stn 03 in the Høgs-

40

Aure et al.: Production enhancement by artificial upwelling

fjord outside the Lysefjord. The artificial upwellingexperiments were executed during the periods 19 Mayto 24 August 2004 and 18 June to 27 August 2005.

Measurements of temperature, salinity, in situ fluo-rescence and turbidity were made and samples ofphytoplankton were gathered weekly from May toJune and from late July to September in 2004, andfrom June to September in 2005. On three 5-d cruises(May/June, August and September) in 2004 and 2005,additional samples were taken for analyses of inor-ganic nutrients (nitrate, nitrite, phosphate and silicate),particulate organic carbon (POC) and chlorophyll a(chl a). To examine the time-scale of the phytoplanktonresponse to the increased supply of nutrients to theeuphotic layer, daily observations were carried out

between 18 and 27 June 2005. Measurements of tem-perature, salinity, in situ fluorescence, turbidity andnutrients on selected stations were also conducted inthe Lysefjord in August 2002, and in the period June toSeptember 2003 (7 dates) and 2006 (10 dates). Samplesfor chl a analysis were filtered onto GF/F filters andstored at –20°C. The samples were analysed fluoro-metrically (Turner Designs-10) according to Parsons etal. (1992) using 90% acetone as solvent and acid cor-rections for phaeopigments. The fluorometer was cali-brated with known concentrations of Sigma chl a(Sigma Chemicals) measured spectrophotometrically.Fluorescence-chl a (FC), turbidity (Seapoint type),salinity and temperature were measured by a CTD(SD 200 W, SAIV A/S). Measurements were recordedevery second while the CTD was lowered at a rate of


1952). Phytoplankton abundance was determinedaccording to Utermöhl (1931) using neutralized forma-lin and Lugol as preservative. Phytoplankton is ex-pressed as biovolume (or plasma volume), i.e. cellvolume minus vacuole volume.

Water currents were measured at depths of 5, 8, 10and 15 m by current meters (SD6000, Sensor Data AS).Current direction and speed were recorded every10 min at Stn 16 from 1 to 20 May and late July to Sep-tember in 2004, and from June to September in 2005.Wind direction and speed were measured at theupwelling platform 5 m above sea level from 21 June to18 August 2005. Subsurface irradiance in the visiblepart of the spectrum (PAR) was obtained with a PUV500 from Biospherical Instruments at vertical profilesdown to depths of 25 to 30 m. Measurements weremade at around local noon at Stns 02 and 03 between22 and 24 June 2005.

RESULTS

Physical conditions

A typical vertical and horizontal salinity distributionof the upper 25 m of the inner part of the Lysefjord isrepresented by the measurements made on 22 July2005 (Fig. 3). From May to September in 2004 and2005, the mean depth of the brackish layer (salinity <25.0 psu) at Stn 11 was 5.0 m (SD = 1.3, n = 18). Withinthe depth interval of 0 to 3 m, where the pump takes itswater, the mean salinity was 14.0 psu (SD = 4.6, n = 18).Below the brackish layer salinity gradually increasedto about 33.0 psu at 30 m depth. From May to Septem-ber temperatures gradually increased from 8.5 to18.0°C in the brackish layer (0 to 5 m), from 7.5 to10.5°C at 10 m and from 7.0 to 8.5°C at 15 m depth.

In 2004 the residual currents (24 h running mean) atdepths between 5 and 15 m at Geitaneset (Stn 16) wereheading out of the fjord, except at the 8 m depth dur-ing late August when residual currents were headinginwards. In 2005 outward currents dominated atdepths of 5, 10 and 15 m, and inwards at 8 m. The 5-dmean current speed between 5 and 15 m depths,before May to September 2004 observation dates,varied between 2.5 and 6.2 cm s–1, and from June toSeptember 2005 between 2.2 and 7.0 cm s–1.

Wind observations at the anchored upwelling plat-form (Fig. 1) in June to August 2005 showed that aninwards wind direction from the west was dominantand the wind speed (24 h running means) variedbetween 0 and 5 m s–1. The exception was a periodfrom 1 to 6 July when the dominant wind direction wasoutwards from the east, with maximum wind speeds(24 h running means) of about 10 m s–1. The strongestcurrents observed during the artificial upwellingperiod in 2005 occurred during this windy period. In2004 there were no current observations at Geitaneset(Stn 16) before 29 May, 6 June and 13 June. Windobservations at a meteorological station just north ofthe Lysefjord showed strong northwesterly winds (10to 15 m s–1) before 29 May and calm weather (


of 14 m at the inlet of the Lysefjord. In the mixing layerof the artificial upwelling between 10 and 30 m, wherethe submerged brackish water rises upwards, themean nutrient values were considerably higher than inthe upper 10 m layer (Table 1). In the 10 to 30 m layerthe elemental ratios (N:Si:Pi = 13:11:1) were quite closeto ratios observed in deep waters in other Norwegianfjords (N:Si:Pi = 11:14:1) (Stigebrandt & Aure 1988).

At Stns 02, 01, 17, 16 and 11, the POC values variedbetween 38 and 517 mg m–3. Maximum values of POCin the water column were found between 3 and 7 m,but the maxima were most frequent at about 7 m. Thehighest POC value of 517 mg m–3 during the upwellingperiod in 2005 was at 7 m at Stn 11 on 17 August. Thehigh correlation between POC and in situ turbidity in2005 (R2 = 0.8, n = 43) shows that the upper 20 m of theLysefjord was dominated by organic particles such asphytoplankton and detritus. In the main artificialupwelling influence layer between 5 and 15 m depth,the R2 between POC and in situ chl a was 0.8, and themean POC:chl a ratio was 80:1 (n = 43).

Intrusion depth and supply of deepwater

The average mixing rate, M* =(Qs/Qb)/(Z30 – Zi), between brackish(Qb, m3 s–1) and seawater (Qs, m3 s–1)from the outlet depth (Z30) to the intru-sion depth (Zi) was estimated as0.8 m–1. On the basis of vertical den-sity profiles in 2004 and 2005, thedensity of the submerged brackish

water and M*, the intrusion depths (Zi) were estimatedto vary between 7 and 11 m in 2004 and 2005, with anaverage of 8 to 9 m. This fits well with the observedmean chl a maximum depth of 7.0 m at Stn 11 duringthe upwelling period from June to September 2005.The total mixing (Qs/Qb) between 30 and 10 m depth atthe platform location was about 14.0. With Qb = 2 m3 s–1

the supply of deeper seawater (Qs) to 10 m depth wasthen 28 m3 s–1. This is about 12% of the total observedmean water exchange between 5 and 15 m depths inthe inner part of the fjord. Based on both the mean con-centrations of nutrients in 2004 and 2005 (Table 1)and the estimated transport of water between 30 to10 m depths, the artificial upwelling supply of nutri-ents was estimated to 450 kg d–1 N, 750 kg d–1 Si and70 kg d–1 Pi.

Primary production rates June 2005

The daily integrated primary production rate be-tween surface and 20 m depths in the Lysefjord at Stn17 on 22 June and at Stn 03 (Fig. 1) on 24 June wereapproximately 350 mg C m–2 d–1. Carbon assimilationrates at fixed depths varied between 0 and 2.8 mg Cm–3 h–1 at Stn 17 and between 0 and 2.3 mg C m–3 h–1

at Stn 03, with the highest values occurring within theupper 0 to 3 m layer. From this we conclude that thedifference in primary production rate between theLysefjord and Høgsfjord was insignificant before theonset of the artificial upwelling in late June 2005 (seeFig. 7a).

Estimated artificial upwelling primary productionrate

The primary production rate (Pupw) measured as kg Cd–1 due to the artificial upwelling is estimated by:

Pupw = PHOSupw· (POC/POP) · R (1)

where PHOSupw (70 kg d–1) is the mean supply of phos-phate to the photic layer due to artificial upwelling,

43

0 5 10 15 20 25

0 0.2 0.4 0.6 0.8 1.2 1.41

Silicate

Nitrate

Orthophosphate

Dep

th (m

)

Pi (mmol m–3)

N and Si (mmol m–3)

10

0

20

30

40

50

Fig. 4. Typical vertical profiles of nitrate (N), silicate (Si) andorthophosphate (Pi) in the inner part of the Lysefjord duringthe artificial upwelling experiments (Stn 17 on 21 June 2005)

Year Depth N Si Pi N/Pi Si/Pi(m) (mmol m–3) (mmol m–3) (mmol m–3)

2004 0–10 0.9 2.1 0.1 6.9 162005 0–10 1.8 4.4 0.3 5.4 13.32004 10–30 10.3 8.1 0.8 13.2 10.42005 10–30 12.7 11.3 0.9 13.9 12.4

Table 1. Mean concentrations of nitrate (N), phosphate (Pi) and silicate (Si)(mmol m–3) and N/Pi, Si/Pi at depths of 0 to 10 m and 10 to 30 m at Stn 11, from

May to September in the Lysefjord in 2004 and 2005


POC/POP = 41 according to the Redfield ratio and R isthe ratio between total and new production; R = 2.3 is atypical value for southern Norwegian marine waters(Wassmann 1990, Skjoldal & Wassmann 1986). UsingEq. (1) Pupw is estimated to be 6600 kg C d–1.

The natural production rate (Pn) measured as kg Cd–1 inside a given area (A, km2) is:

Pn = pn· A (2)

where pn is the average primary production rate per m2

below the upper brackish layer. The total primary pro-duction rate (PT) is then the sum of Pupw and Pn, sincethe water and related natural phytoplankton exchangewith the external fjord system is not significantly influ-enced by the artificial upwelling (see previous expla-nation). Typical mean daily integrals of carbon assimi-lation in the euphotic zone in fjords for the period fromApril to September are 500 to 600 mg C m–2 d–1, withabout one-half occurring below the upper brackishlayer (pn = 300 mg C m–2 d–1) (Erga 1989b, Erga et al.2005).

The area of influence (Ainfl) is defined as the areawhere the phytoplankton biomass and the primaryproduction rate are significantly stimulated by the arti-ficial upwelling. Investigation of the longitudinal dis-tribution of chl a in the Lysefjord during artificialupwelling in 2004 and 2005 (Fig. 5a) showed that in allcases, except on 29 May 2004 and 6 June 2005, thearea of influence was 10 km2 or less, e.g. inside Stn 01(Fig. 1). On 29 May and 6 June 2005 currents andwater exchange were considerably increased and agreater proportion of chl a existed outside the area of10 km2. On basis of these observations our main fixedobservation area (Ao) is selected to be the inner 10 km2

of the Lysefjord (Fig. 1). Using A = Ao in Eq. (2), thenatural production (Pn) is estimated to be 3000 kg C.The total primary production rate PT = Pupw + Pn causedby the increased supply of nutrients to the euphoticlayer is then calculated to be 9600 kg C d–1, i.e. anincrease of the primary production rate (PT/Pn) by afactor of about 3.

In a steady-state situation the total upwelling pri-mary production rate (PT) measured as kg C d–1 insideAo is balanced with the transport of carbon (Qv · Cmupw)leaving Ao, where Qv is the water transport in the layerinfluenced of the artificial upwelling and Cmupw is themean carbon concentration inside Ao, i.e.

PT = Qv · Cmupw (3)

With Cmupw = CTupw/(Ao· Ha) we get:

PT = ChlTupw /(Ao· Ha) · Qv · (POC/chl a) (4)

where CTupw and ChlTupw are the total carbon andchl a inside Ao, Ha is the mean thickness of the plank-ton layer influenced by the artificial upwelling and

POC/chl a is the ratio between particulate organiccarbon and chl a. The total chl a inside Ao (ChlTupw,measured as kg chl a) is then:

ChlTupw = PT · (Ao· Ha) /(POC/chl a)/Qv (5)

This relation shows that ChlTupw inside Ao is alsoexpected to increase by a factor of 3 during the artifi-cial upwelling experiment.

Observed effects of artificial upwelling

Mean chl a values in the 4 to 15 m layer at Stn 11 inthe inner part and at Stn 2 in the middle of the Lyse-fjord (Fig. 1) were, respectively, 1.7 mg m–3 (SD = 0.7,n = 335) and 1.6 mg m–3 (SD = 0.6, n = 335,) during theMay to September periods from 2002 to 2006, exclud-ing the artificial upwelling periods in 2004 and 2005.Chl a values in the range 1 to 2 mg m–3 are typical forthe upper 10 m of the water column in fjords duringsummer when nutrients are scarce (Aure et al. 2000).This confirms that the horizontal differences of chl abetween the inner and middle fjord are insignificantduring natural conditions. To examine the effects ofthe artificial upwelling experiment, observed chl a wasintegrated in the 4 to 15 m layer within Ao, both in

44

25

20

15

10

5

0Stn 11 Stn 16 Stn 17 Stn 01

Dep

th (m

)

250 1 2 3 4 5 6 7 8 9 10

20

15

10

5

0

Dep

th (m

)


situations with (ChlTupw) and without (ChlTn) artificialupwelling. Examples of typical vertical distributions ofchl a inside Ao both with artificial upwelling and dur-ing natural conditions are shown in Fig. 5.

In 2004 the artificial upwelling was started on 19May. After a period with strong northerly winds andcurrents in late May, weather conditions becamecalmer, and ChlTupw values increased from 167 kg on29 May to 400 to 500 kg in June (Fig. 6a). On 27 Julyand 3 August ChlTupw was still at the same level as inJune. On 17 August ChlT was reduced to about 130 kgeven though the current and wind conditions were stillmoderate. This anomalously low value was related to acollapse in the diatom stock inside Ao (discussed later).The artificial upwelling system stopped on 24 August.After this date the integrated chl a inside Ao decreasedto about 100 kg. In the artificial upwelling period from6 June to 3 August 2004 the mean ChlTupw was about480 kg (48 mg m–2), excluding 29 May 2004 when Ainflwas much greater than Ao, and the diatom collapse on17 August 2004. The mean chl a concentration(chlmupw) inside Ao was 4.8 mg m–3. Outside the

upwelling period in May and late August to September2004 the mean ChlTn was 155 kg (15.5 mg m–2) and themean chl a concentration (chlmn) was 1.9 mg m–3

inside Ao. ChlTupw then increased by a factor of about3.0 and chlmupw increased by a factor of about 2.5 inthe artificial upwelling period from June to the firstpart of August 2004.

In 2005 the artificial upwelling was started on 18June and was closed down on 27 August. The daily ob-servations during the first week of upwelling (Fig. 7a)showed that chl a integrated between the surface layerand 15 m depth (ChlI, mg m–2) at Stn 11 inside Aoincreased from 20 mg m–2 on 18 June to a maximum of60 to 70 mg m–2 on 25–26 June. The time needed toestablish a fully developed artificial upwelling, thus,appears to be about 1 wk. During this period ChlI atStn 11 increased by a factor of about 3 relative to Stn 02outside Ao, and the mean daily increase of ChlI after21 June was about 23%.

During the period from 26 June to 25 August 2005,while the artificial upwelling was in progress, ChlI (mgm–2) values were significantly higher at Stn 11 than atthe reference station, Stn 02 (Fig. 7b). At Stn 11, ChlIvaried between 53 and 73 mg m–2, with the exception

45

Fig. 6. Integrated chl a (ChlT, kg) from below the surfacelayer to 15–20 m depth inside Ao (= 10 km2) in the inner partof the Lysefjord. (a) 8 May to 4 September 2004 and (b) 18June to 5 September 2005 (grey columns and horizontal arrow= artificial upwelling response periods, black columns = nat-ural conditions, hatched column = phytoplankton [diatom]

collapse on 17 August 2004)

Fig. 7. (a) Vertical integrated chl a (mg m–2) at Stns 11 and 02during the period 18 to 27 June 2005 (artificial upwellingcommenced on 18 June). (b) Vertically integrated chl a (mgm–2) at Stns 11 and 02 from 18 June to 5 September 2005(horizontal arrow = artificial response upwelling period)


of 6 July when ChlI was reduced to 23 kg due to a con-siderable increase in out-fjord wind speed and conse-quently higher water exchange (Ainfl >> Ao). At the ref-erence station (Stn 02) ChlI varied between 15 and30 mg m–2 in the same period. Mean ChlI values atStn 11 (excluding 6 July when Ainfl >> Ao) and Stn 02during the artificial upwelling period were about 60and 20 mg m–2, respectively. The mean chl a concen-tration (chlm) showed a similar pattern as ChlI, and atStn 11 it varied between 5.3 and 10.5 mg m–3, with theexception of 6 July where chlm was 3.3 mg m–3. AtStn 02 chlm varied between 1.7 and 3.3 mg m–3. Theaverage chlm was 6.5 mg m–3 at Stn 11 and 2.2 mg m–3

at Stn 02. Both mean ChlI and chlm inside Ao werethen about 3 times as high at Stn 11 as at the referencestation, Stn 02. In the artificial upwelling period thetypical thickness of the phytoplankton layer (Ha) andthe mean chl a maximum depth at both Stn 11 and 02were 9 to 10 m and 7 m, respectively.

In the upwelling period from 26 June to 25 August2005 the integrated chl a inside Ao (ChlTupw) variedbetween 410 and 675 kg, except on 6 July when Ainflwas much greater than Ao (Fig. 6b). The mean ChlTupw,excluding 6 July (Ainfl >> Ao), was 510 kg (51 mg m–2)and the mean chl a concentration (chlmupw) was 5.3 mgm–3. During natural conditions, the integrated chl ainside Ao (ChlTn) was 163 kg (16 mg m–2) and the meannatural chl a concentration (chlmn) was 1.7 mg m–3.Both ChlTupw and chlmupw inside Ao increased, there-fore, by a factor of about 3 in the artificial upwellingperiod from June to August 2005. The observed meannatural ChlTn of 160 kg between the 4 and 15 m depthsin 2004 and 2005 was almost identical to the observedmean ChlTn of 165 kg (SD = 35 kg, n = 16) at Stns 11,16, 17 and 01 inside Ao from May to September in 2002,2003 and 2006.

Fig. 8 shows that there is a high correlation betweenobserved ChlT inside Ao and the water transport (Qv,m3 s–1). ChlTupw, and the difference between ChlTupwand ChlTn are decreasing with increasing Qv and withthe largest relative changes appearing at low Qv.When Qv is less than 260 m3 s–1 the observed influencearea of the artificial upwelling is less than Ao = 10 km2.The mean total primary production rate (PT) inside Ao(Ainfl ≤ Ao) during artificial upwelling is calculatedusing the observed mean of ChlTupw (500 kg) and Qv(235 m3 s–1) in Eq. (4). Natural production, Pn, is calcu-lated using ChlTn = 180 kg and the related mean Qv =225 m3 s–1. When Ha = 9 m and POC/chl a = 80, PT andPn are estimated to be approximately 9000 kg C d–1

(900 mg C m–2 d–1) and 3000 kg C d–1 (300 mg C m–2

d–1), respectively. PT and Pn measured as kg C d–1mayalso be expressed as:

PT (Pn) = k · ChlTupw (n) (6)

where k is the photosynthetic effectiveness (daily inte-grals of vertically integrated carbon assimilation overchl a, mg C mg chl a–1 d–1) (Prasad et al. 1995, Erga etal. 2005) and ChlTupw (n) is the mean total chl a insideAo. Possible losses of chl a due to sedimentation are nottaken into account, but they are probably low undercontinuous upwelling and stratified conditions (Riebe-sell 1989). The restricted residence time of the phyto-plankton layer (5 d) inside Ao and the low sinkingvelocity of healthy algae (


Phytoplankton composition

Some days before the artificial upwelling started on19 May 2004, the phytoplankton stock inside the areaof influence of artificial upwelling was dominated bydinoflagellates (Fig. 9a). During June and in the firstpart of August 2004 there was a considerable relativeincrease of diatoms with Chaetoceros spp. as the dom-inant genus. The diatom biomass increased from about4% of the total phytoplankton biovolume (sum ofdiatoms and flagellates) on 29 May to about 41% on 13June. During this period the diatom volume biomassincreased by 20% d–1. On 3 August the diatom biovol-ume still constituted 84% of the total biovolume insideAo. Outside Ao at Stn 02, and in the adjacent Høgsfjord(Stn 03), no diatoms were observed. Here, flagellatesincluding dinoflagellates were the dominant group ofphytoplankton in terms of biomass. On 17 August the

diatom stock was greatly reduced. After the artificialupwelling was stopped in late August, flagellates


DISCUSSION

Physical controls on primary production rate

The large-scale experiment in the Lysefjord showedthat artificial upwelling enhanced the observed algaebiomass and the estimated primary production ratewithin an area of about 10 km2 during summers in 2004and 2005. The artificial upwelling also stimulateddiatom growth. These results are in accordance withmodel simulations of primary production rate in a sim-ilarly scaled fjord subjected to different scenarios ofsubmerged freshwater discharge (Berntsen et al.2002). Our study is the first full-scale experiment to usesubmerged brackish water discharged in a controlledmanner to force artificial upwelling in a fjord area andto demonstrate experimentally the significant potentialfor ecological studies on this topic in fjords.

Previous investigations in western Norwegian fjordshave revealed a remarkable consistency with respectto water exchange processes and phytoplanktongrowth dynamics (Erga & Heimdal 1984, Erga 1989a,b,Erga et al. 2005). Nutrient limitation usually leads toreduced primary production yields and changes inspecies composition to a predominance of ultraplank-ton (< 5 µm) flagellates and dinoflagellates during thesummer period, but still more than 50% of the annualprimary production occurs after the spring diatomblooms. The mean total primary production rate belowthe surface brackish layer due to artificial upwelling(PT) was determined to be about 900 mg C m–2 d–1

inside an area of 10 km2, about 3 times the natural pro-duction rate (Pn). A primary production rate in theeuphotic zone of 1500 mg C m–2 d–1 is often found inwestern Norwegian fjords during the main springbloom in March (Erga & Heimdal 1984, Erga et al.2005). Therefore, it ought to be possible to increase pri-mary production rate rates in the Lysefjord to 1500 mgC m–2 d–1 during summer by forced upwelling of nutri-ent rich deeper water. A considerable enhancement ofprimary production rates due to natural upwellinghave also been reported for many of the strong naturalupwelling systems in the world, e.g. the northwestcoast of South Africa (Brown 1992), northcentral Chile(Rutllant & Montecino 2002) and northwestern Spain(see Álvarez-Salgado et al. 2005). Maximum primaryproduction rates for these highly productive waters aretypically 6000 to 8000 mg C m–2 d–1, considerablehigher than primary production rates during the springbloom in Norwegian fjord waters.

A nutrient enrichment experiment using mesocosms(plastic cylinders) in Lindåspollene, a landlocked fjordsystem north of Bergen (Aksnes et al. 1985), demon-strated that an artificial upwelling rate correspondingto approximately 1 m d–1 resulted in an 8 to 10-fold

increase in the midsummer primary production rate.The upwelling rate inside Ao (10 km2) in this experi-ment was approximately 0.3 m d–1, and with anobserved production enhancement factor of about 3,this relationship is in accordance with the study ofAksnes et al. (1985).

The observed mean water exchange between 5 and15 m (Qvm) during the artificial upwelling periods(Ainfl ≤ Ao) in the inner part of the Lysefjord was about240 m3 s–1, which gives a mean residence time (Tr) ofabout 5 d in the inner 10 km2 of the fjord. The time-scale of the phytoplankton response to increased sup-ply of nutrients to the euphotic layer in June 2005 wasobserved to be 5 to 7 d (Fig. 7a), which is similar to themean residence time estimated. The area of influenceof increased production based on artificial upwelling isdependent on both the residence time of the phyto-plankton layer (Tr) and the phytoplankton division rate(Ar). According to Aksnes (1993), the condition for alocal or regional effect on new production is depen-dent upon the ratio R = 1/(Tr · Ar). When R is much lessthan 1 the new production will be local. In the inner10 km2 of the Lysefjord, R was 0.2 using Ar = 1 d–1. Thisindicates that most of the artificial upwelling produc-tion took place inside the fixed observation area Ao of10 km2. Observations of the longitudinal distribution ofchl a in the Lysefjord during artificial upwelling in2004 and 2005 support this assumption.

To estimate the area of influence (Ainfl) of artificialupwelling in a fjord system we use a combination ofEqs. (4, where Ao = Ainfl, measured in km2) & (6):

Ainfl = (CTupw/ChlTupw) · Qv/(k · Ha) (7)

where Ha is the mean thickness (m) of the phytoplank-ton layer, CTupw and ChlTupw are the total particulateorganic carbon and chl a biomass, respectively, insideAinfl, Qv is the water flux out of the phytoplankton layerand k is the is the photosynthetic effectiveness in thephytoplankton layer. CTupw/ChlTupw is the ratiobetween total particulate organic carbon and chl a (i.e.POC/chl a). It follows that Ainfl is proportional to themean water exchange Qv and inversely proportional tok when Ha and POC/chl a are considered as constants.Water flux, Qv, is associated with the residence time ofthe phytoplankton layer (Tr) inside Ainfl, and k with thephytoplankton division rate (Ar) (see previously). Themean chl a concentration (chlmupw) inside the Ainfl isdetermined by Eqs. (1), (2) & (7):

chlmupw = Pupw· [(chl a/POC)/Qv] + [Pn/(k · Ha)] (8)

In Fig. 10 chlmupw is calculated as a function of Qvusing Pupw = 6600 kg C d–1, POC/chl a = 80, Ha = 10 m,Pn = 300 mg C m–2 d–1 and k = 18 mg C mg chl a–1 d–1.A mean POC/chl a ratio of 81 (n = 288) was typical foranother western Norwegian fjord during the summer

48


period (Erga et al. 2005). The observed mean chlmupwand Qv inside Ao in 2005 were 5.3 mg m–3 and 235 m3

s–1, respectively. As shown in Fig. 10, the observedchlmupw was well in agreement with the calculatedvalue of 5.7 mg m–3 when Qv = 235 m3 s–1. As observed,the calculated Ainfl was less than 10 km2 when Qv wasbelow 260 m3 s–1. During natural conditions (Pupw = 0)the mean chl a concentration (chlmn) inside the Ainfl iscalculated to be 1.7 mg m–3 (Fig. 10), almost identicalto the observed chlmn during natural conditions in2004 and 2005 (1.8 mg m–3). When the primary produc-tion rates due to the artificial upwelling (Pupw) areincreased by factors of 1.5 and 2.0, chlmupw is increasedto 7.8 and 9.8 mg m–3, respectively, when Qv = 235 m3

s–1. A doubling of Pupw represents a mean daily inte-grated carbon assimilation of about 1.6 g C m–2 d–1,which is at the same level as the daily integrated car-bon assimilation during the main spring bloom in otherwestern Norwegian fjords (Erga & Heimdal 1984, Erga1989b, Erga et al. 2005). This level is within the naturalvariability of the fjord ecosystem and probably a rea-sonable upper limit of enhanced primary productionachieved by artificial upwelling.

The k value of 18 mg C mg chl a–1 d–1 used in our cal-culations is typical for a chl a maximum at about 10 mdepth during the summer in western Norwegian fjords(S. R. Erga unpubl. data). A shallower intrusion depth(Zi) will result in a higher k value, since the POC/chl a ra-tio increases upward in the water column during strati-fied conditions as light conditions improve (Erga1989a,b). In periods with persistent low solar irradianceat the surface and/or increased upper layer turbidity, we

expect lower k values and, thus, a reduced total primaryproduction rate (PT) (Eq. 6) and increased area of influ-ence (Ainfl) (Eq. 7). In a comprehensive primary produc-tion rate investigation on the Iberian shelf break (north-western Spain) during periodic upwelling andrelaxation events in June through July, k values werefound to be within the range 9 to 24 mg C mg chl a–1 d–1

(primary production rate and chlorophyll concentration,depth-integrated from surface to the base of euphoticzone) (Joint et al. 2002). From their data a mean k valueof 16 mg C mg chl a–1 d–1 can be calculated. However,during a winter upwelling/downwelling sequence in theRía de Vigo (northwestern Spain), a bloom of Skele-tonema costatum revealed k values as high as 45 mg Cmg chl a–1 d–1 (Álvarez-Salgado et al. 2005).

Species succession

Physical conditions for large-scale blooms of diatomstypically include persistent upwelling regimes (Brown1992, Taylor & Haigh 1996, Rutllant & Montecino 2002,Trainer et al. 2002, Ning et al. 2004, Álvarez-Salgadoet al. 2005), and dinoflagellate blooms occur mostfrequently in stratified waters (Delmas et al. 1993,Reguera et al. 1995, Taylor & Haigh 1996). Common formany of these upwelling systems is that the growthstimulating response seems to occur towards the end ofthe upwelling period or beginning of the relaxationperiod when the water column start to stabilize andnutrients are replenished. In the Lysefjord a modestartificial upwelling was achieved in both 2004 and2005, with a mean intrusion depth of 8 to 9 m. It iswidely accepted that the coupling between internalbiological processes and external physical perturba-tions plays a key regulatory role in the seasonalsuccession of phytoplankton (Harris & Trimbee 1986,Taylor & Haigh 1996, Teira et al. 2001).

According to the ‘intermediate disturbance hypothe-sis’ (IDH), intermediate disturbance or turbulence willlead to maximum species diversity of phytoplankton(see Sommer 1995), while intense disturbances reducediversity to a few dominant species (Flöder & Sommer1999, Huisman et al. 1999). Besides increased produc-tion, it was desirable to obtain a dominance of ‘healthy’diatoms in our artificial upwelling experiments. Oneprecondition for this is to ensure that sufficient concen-trations of ‘seed’ populations are present in the initialphase of the artificial upwelling at the operationaldepth of the system (Ishizaka et al. 1983), and that abalance between nutrient supply and the dilution ofgrowing diatoms is obtained. According to Hutchinson(1953), changes in the physical regime on time scaleslonger than the generation time of the organism, whichfor phytoplankton is about 1 ± 0.5 d–1, should prevent

49

0123456789

10111213141516

140 170 200 230 260 290 320 350 380 410 440 470 500

Qv (m3 s–1)

Chl

m (m

g m

–3)

0

2

4

6

8

10

12

14

16

18

20

Ain

fl (k

m2 )

Pupw

AinflPupw = 0

2 x Pupw1.5 x Pupw

x

Fig. 10. Calculated area of influence (Ainfl) and mean chl a(chlm) inside the area of influence as a function of watertransport (Qv). POC/chl a = 80, Ha = 10 m, k = 18 mg C mg chla–1 d–1, Pn = 300 mg C m–2 d–1 and Pupw = 6600 kg C d–1. Thefollowing cases are shown: Pupw = 0, Pupw × 1, Pupw × 1.5 andPupw × 2.0. Mean observed chlm and Qv (shown by x) duringartificial upwelling in 2005 inside Ao = 10 km2 (Ainfl < Ao)


competitive exclusion. The main advective processesin the inner 10 km2 of the Lysefjord have been shownto operate on a much longer time scale than this (5 to7 d). The retention time should, therefore, be sufficientfor a diatom bloom to develop within the main area ofartificial upwelling. The artificial upwelling watertransport and associated ‘turbulence’ was insignificantcompared with natural water exchange (12%). Basedon this we do not expect any effects of the artificialupwelling water transport on selection of diatoms.

At the head of the Lysefjord, the daily integral of car-bon assimilation with Emiliania huxleyi as the domi-nant species was no higher than 350 mg C m–2 d–1 inJune 2005, even if cell concentrations were as high as10 to 12 × 106 cells l–1. However, such a low rate of car-bon assimilation is not representative of the artificialupwelling period, since it only concerns the initial partwhen no stimulating effect on primary production ratehas been obtained. Previous experience has shownthat when natural upwelling in fjords occurs duringsummer, daily integrals of carbon assimilation of about1 g C m–2 d–1 could be achieved (Erga 1989b), and thatsuch events may stimulate diatom growth (Aksnes etal. 1985, Paasche & Erga 1988, Erga 1989a). Silicate isan important competitive factor in this context (Egge &Aksnes 1992). Our results for the Lysefjord are inaccordance with these findings. The dominance ofdiatoms, however, was higher in 2004 than in 2005, asrevealed by their accounting for 90% and 60%,respectively, of the total biovolume by the end of July.This could be ascribed to the mass occurrence of Emil-iania huxleyi in the whole fjord system from mid-Juneuntil mid-July 2005, which resulted in unfavourablelight conditions due to high concentrations of detachedcoccoliths in the water column. Typical of such situa-tions are increased scattering to absorption ratios(Frette et al. 2004). It is also interesting to note that bythe end of July 2005, Skeletonema sp. was the majorcontributor to phytoplankton biomass within the areaof influence of the artificial upwelling, while outsidethis area it was almost absent.

In both 2004 and 2005 the diatom stock was greatlyreduced during August (Fig. 9). Possible explanationsfor the diatom breakdown could be a lack of ‘seed’diatoms in the influence region or an incidental unbal-ance between nutrient supply and diatom biomass.From mid-August 2004 the currents within the area ofinfluence increased, which led to higher rates of waterexchange. The effect of this may have been a reducedphytoplankton biomass due to dilution. The phyto-plankton may, therefore, have adapted to reduced butstable nutrient concentrations, and to less favourablelight conditions. Also, diatoms were scarce outside thearea of influence both in August 2004 and 2005. There-fore, if the efficiency of the artificial upwelling, as far

as diatom growth is concerned, depends on ‘seed pop-ulations’ from outside, lower levels of diatoms are to beexpected under such conditions (Ishizaka et al. 1983).

The normal seasonal succession pattern of phyto-plankton in fjords of western Norway involves a risingincidence of toxic dinoflagellates in the upper brackishlayer from June to September (Dahl et al. 2004, Erga etal. 2005), among which Dinophysis species are mostcommon. Members of the potentially toxic diatomgenus Pseudonitzschia (Scholin et al. 2000) are oftenencountered below the pycnocline in June. This wasalso the case in the Lysefjord. These 2 genera are alsocommon during the summer in coastal waters through-out the world, and are known to cause problems for themussel industry (Belin 1993, Reguera et al. 1995, Auneet al. 1996, Taylor & Haigh 1996, Horner et al. 1997,Ryan et al. 2005, Strohmeier et al. 2005).

When Pseudonitzschia spp. occur in western Norwe-gian fjords, they are always accompanied by a severalother nontoxic diatoms, of which Leptocylindrus spp.,Chaetoceros spp. and Skeletonema sp. are the mostcommon (see Erga & Heimdal 1984, Erga 1989a, Erga& Skjoldal 1990). Representatives of these genera alsomade up the largest fraction of diatoms in the Lysefjordduring the artificial upwelling period. To date,Pseudonitzschia spp. has not caused any toxicity prob-lems in Norwegian fjords.

In conclusion, the large-scale experiment in theLysefjord during summers of 2004 and 2005 demon-strated that artificial upwelling of nutrients fromdeeper water strata approximately tripled mean algaebiomass and the estimated primary production ratebelow the surface layer within an influence area of10 km2 at the head of the fjord. The concentrations andcomposition of the upwelling nutrients are identical tothose normally encountered during the winter andspring seasons. There were differences in the speciescomposition of the algae within and outside the area ofinfluence, with periodic dominance of diatoms insidethe influence area. However, diatom growth seems tobe dependent upon ‘seed populations’ in the adjacentfjord waters. The increase in primary production ratedue to artificial upwelling should occur within the nat-ural variability of the fjord ecosystem and be confinedto the area of interest. A higher stable level of phyto-plankton biomass, dominated by nontoxic species, islikely to increase the fjord’s carrying capacity ofseston-feeding shellfish and could form the basis ofmore predictable mussel cultivation in fjords. To inves-tigate this possibility further, a study of the effects oflarge-scale artificial upwelling on commercial musselproduction has now been launched in the Lysefjord. Itwill also focus more thoroughly on the ecologicalaspects of artificial upwelling, including implementa-tion of a 3D physical/biological model.

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Acknowledgements. This work was supported by CountyCouncil of Rogaland, Norwegian Shellfish Production AS,Lyse Energy AS, Haugalandsrådet and Institute of MarineResearch. We thank the crews of RV ‘Hans Brattstrøm’ andRV ‘G. M. Dannevig’ for their kind assistance during thecruises. Special thanks go to G. Mykletun for valuable projectsupport, O. M. Gjervik for valuable help during the cruises,and to E. O. Strohmeier for assistance in collecting databetween the cruises.

LITERATURE CITED

Aksnes DL (1993) Sammenfatning av resultater – en vurder-ing av årsaker. Sluttrapport Prymnesium parvum iRyfylke. SMR-rapport 9/93, Universitetet i Bergen, Senterfor Miljø- og Ressursstudier, Bergen, Norway

Aksnes DL, Magnesen T, Lie U (1985) Nutrient enrichmentexperiments in plastic cylinders and the implications ofenhanced primary production rate in Lindåspollene, west-ern Norway. Sarsia 70:45–58

Aksnes DL, Aure J, Kaartvedt S, Magnesen T, Richard J(1989) Significance of advection for the carrying capacitiesof fjord populations. Mar Ecol Prog Ser 50:263–274

Álvarez-Salgado XA, Niet-Cid M, Piedracoba S, Crespo BGand others (2005) Origin and fate of a bloom of Skele-tonema costatum during a winter upwelling/downwellingsequence in the Ría de Vigo (NW Spain). J Mar Res 63:1127–1149

Asplin L, Salvanes AG, Kristoffersen JB (1999) Nonlocal winddriven fjord coast advection and its potential effect onplankton fish recruitment. Fish Oceanogr 8:255–263

Aune T, Strand Ø, Aase B, Weidemenn J, Dahl E, Hovgaard P(1996) The Sognefjorden, a possible location for musselfarming? In: Yasumoto T, Oshima Y, Fukuyo Y (eds)Harmful and toxic algal blooms. IntergovernmentalOceanographic Commission of UNESCO, p 73–75

Aure J, Molvær J, Stigebrandt A (1996) Observations ofinshore water exchange forced by a fluctuating offshoredensity field. Mar Pollut Bull 33:112–119

Aure J, Erga SR, Asplin L (2000) Increased biological produc-tion in fjords by artificial upwelling. Fisken og Havet (InstMar Res Bergen) 11:1–30

Belin C (1993) Distribution of Dinophysis spp. and Alexan-drium minutum along French coasts since 1884 and theirDSP and PSP toxicity levels. In: Smayda TJ, Shimizu Y(eds) Toxic phytoplankton blooms in the sea. Elsevier,Amsterdam, p 469–474

Berntsen J, Aksnes DL, Foldvik A (2002) Production enhance-ment by artificial upwelling — a simulation study. Hydro-biologia 484:177–190

Brown PC (1992) Spatial and seasonal variation in chlorophylldistribution in the upper 30 m of the photic zone in thesouthern Benguela/Agulhas ecosystem. S Afr J Mar Sci12:515–525

Dahl E, Aune T, Tangen K, Castberg T, Gustad E and others(2004) Giftalger og algegifter i norske farvann — erfaringerfra de siste fem årene. In: Sjøtun K (ed) Fisken og havet(Inst Mar Res Bergen), p 91–95

Delmas D, Herbland A, Maestrini SY (1993) Do Dinophysisspp. come from the ‘open sea’ along the French Atlanticcoast. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplanktonblooms in the sea. Elsevier, Amsterdam, p 489–494

Dugdale RC, Goering JJ (1967) Uptake of new and regener-ated forms of nitrogen in primary productivity. LimnolOceanogr 12:196–206

Egge JK, Aksnes DL (1992) Silicate as regulating nutrient in

phytoplankton competition. Mar Ecol Prog Ser 83:281–289Eilertsen HC, Taasen JP (1984) Investigations on the plankton

community of Balsfjorden, northern Norway. The phyto-plankton 1976–1978. Environmental factors, dynamics ofgrowth, and primary production rate. Sarsia 69:1–15

Erga SR (1989a) Ecological studies on the phytoplankton ofBoknafjorden, western Norway. I. The effect of waterexchange processes and environmental factors on tempo-ral and vertical variability of biomass. Sarsia 74:161–176

Erga SR (1989b) Ecological studies on the phytoplankton ofBoknafjorden, western Norway. II. Environmental controlof photosynthesis. J Plankton Res 11:785–812

Erga SR, Heimdal BR (1984) Ecological studies on the phyto-plankton of Korsfjorden, western Norway. The dynamicsof a spring bloom seen in relation to hydrographical condi-tions and light regime. J Plankton Res 6:67–90

Erga SR, Skjoldal HR (1990) Dial variations in photosyntheticactivity of summer phytoplankton in Lindåspollene, west-ern Norway. Mar Ecol Prog Ser 65:73–85

Erga SR, Aursland K, Frette Ø, Hamre B and others (2005) UVtransmission in Norwegian marine waters: controlling fac-tors and possible effects on primary production rate andvertical distribution of phytoplankton. Mar Ecol Prog Ser305:79–100

Figueiras FG, Labarta U, Rernández Reiriz MJ (2002) Coastalupwelling, primary production rate and mussel growth inthe Rías Baixas of Galicia. Hydrobiologia 484:121–131

Flöder S, Sommer U (1999) Diversity in planktonic communi-ties: an experimental test of the intermediate disturbancehypothesis. Limnol Oceanogr 44:1114–1119

Frette Ø, Erga SR, Hamre B, Aure J, Stamnes JJ (2004) Sea-sonal variability in inherent optical properties in a westernNorwegian fjord. Sarsia 89:276–291

Harris GP, Trimbee AM (1986) Phytoplankton dynamics of asmall reservoir: physical/biological coupling and the timescales of community change. J Plankton Res 8:1011–1025

Horner RA, Garrison DL, Plumley FG (1997) Harmful algalblooms and red tide problems on the U.S. west coast. Lim-nol Oceanogr 42:1076–1088

Huisman J, van Ostveen P, Weissing FJ (1999) Speciesdynamics in phytoplankton blooms: incomplete mixingand competition for light. Am Nat 154:46–68

Hutchinson GE (1953) The concept of pattern in ecology. ProcAcad Nat Sci Phila 105:1–11

Ishizaka J, Takahashi M, Ichimura S (1983) Evaluation ofcoastal upwelling effects on phytoplankton growth bysimulated culture experiments. Mar Biol 76:271–278

Joint I, Groom SB, Wollast R, Chou L and others (2002) Theresponse of phytoplankton production to periodic up-welling and relaxation events at the Iberian shelf break:estimates by the 14C method and by satellite remotesensing. J Mar Syst 32: 219–238

Mann KH, Lazier JRN (1996) Dynamics of marine ecosystems:biological–physical interactions in the oceans. BlackwellScience, Malden, MA

McClimans TA, Eidnes G, Aure J (2002) Controlled artificialupwelling in a fjord using submerged fresh water dis-charge: computer and laboratory simulations. Hydrobiolo-gia 484:191–202

Morikawa T (2001) Stock enhancement of marine livingresources in Japan’s coastal water. ASEAN-SEAFDECMillenium Fisheries Exhibition, 11–24 Nov 2001

Ning X, Chai F, Xue H, Cai Y, Liu C, Shi J (2004)Physical–biological oceanographic coupling influencingphytoplankton and primary production rate in theSouth China Sea. J Geophys Res 109:C10005, doi:10.1029/2004JC002365

51


Olsen YT (2002) MARICULT Research Programme: back-ground, status and main conclusions. Hydrobiologia 484:1–10

Paasche E (1988) Pelagic primary production rate innearshore waters. In: Blackburn TH, Sørensen J (eds)Nitrogen cycling in coastal marine environments. JohnWiley & Sons, Chichester, p 33–57

Paasche E, Erga SR (1988) Phosphorus and nitrogen limitationof phytoplankton in the inner Oslofjord (Norway). Sarsia73:229–243

Parsons TR, Maita Y, Lalli CM (1992) A manual of chemicaland biological methods for sea water analysis. PergamonPress, New York

Pitcher GC, Calder D (1998) Shellfish mariculture in theBenguela system: phytoplankton availability of food forcommercial mussel farms in Saldanha Bay. J Shellfish Res17:15–24

Prasad KS, Lohrenz SE, Redalje DG, Fahlnenstiel GL (1995)Primary production rate in the Gulf of Mexico using a‘remotely-sensed’ trophic category approach. Cont ShelfRes 15:1355–1368

Reguera B, Bravo I, Fraga S (1995) Autoecology and some lifehistory stages of Dinophysis acuta Ehrenberg. J PlanktonRes 17:999–1015

Riebesell U (1989) Comparison of sinking and sedimentationrate measurements in a diatom winter/spring bloom. MarEcol Prog Ser 54:109–119

Rutllant J, Montecino V (2002) Multiscale upwelling forcingcycles and biological response off north-central Chile. RevChil Hist Nat 75:217–231

Ryan JP, Chavez FP, Bellingham JG (2005) Physical–biologi-cal coupling in Monterey Bay, California: topographicinfluences on phytoplankton ecology. Mar Ecol Prog Ser287:23–32

Ryther JH (1969) Photosynthesis and fish production in thesea. Science 166:72–76

Scholin CA, Gulland F, Doucette GJ, Benson S and others(2000) Mortality of sea lions along the central Californiacoast linked to a toxic diatom bloom. Nature 403:80–84

Skjoldal HR, Wassmann P (1986) Sedimentation of particulateorganic matter and silicium during summer in Lindåspol-

lene, Western Norway. Mar Ecol Prog Ser 30:49–63Skjoldal HR, Dalpadado P, Dommasnes A (2004) Food

webs and trophic interactions. In: Skjoldal HR, Sætre R,Fernö A, Misund OA, Røttingen I (eds) The NorwegianSea ecosystem. Tapir Academic Press, Trondheim,p 447–506

Smith WO, Heburn GW, Barber RT, O’Brien JJ (1983) Regula-tion of phytoplankton communities by physical processesin upwelling ecosystems. J Mar Res 41:539–556

Sommer U (1995) An experimental test of the intermediatedisturbance hypothesis using cultures of marine phyto-plankton. Limnol Oceanogr 40:1271–1277

Steemann Nielsen E (1952) The use of radio-active carbon(14C) for measuring organic production in the sea. J ConsPerm Int Expl Mer 18:117–140

Stigebrandt A, Aure J (1988) Observations on plant nutrientsin some Norwegian fjords. Sarsia 74:303–307

Strohmeier T, Aure J, Duinker A, Castberg T, Svardal A,Strand Ø (2005) Flow reduction, seston depletion, meatcontent and distribution of diarrhea shellfish toxins in along-line blue mussel (Mytilus edulis) farm. J Shellfish Res24:15–23

Taylor FJR, Haigh R (1996) Spatial and temporal distributionof microplankton during the summers of 1992–1993 inBarkley Sound, British Columbia, with emphasis on harm-ful species. Can J Fish Aquat Sci 53:2310–2322

Teira E, Serret P, Fernández E (2001) Phytoplankton size-structure, particulate and dissolved organic carbon pro-duction and oxygen fluxes through microbial communitiesin the NW Iberian coastal transition zone. Mar Ecol ProgSer 219:65–83

Trainer VL, Hickey BM, Horner RA (2002) Biological andphysical dynamics of domoic acid production off theWashington coast. Limnol Oceanogr 47:1438–1446

Utermöhl H (1931) Neue Wege in der quantitativen Erfassungdes Planktons. (Mit besonderer Berücksichtigung desUltraplanktons). Verh Int Verein Theor Angew Limnol 5:567–596

Wassmann P (1990) Relationship between primary and exportproduction in the boreal coastal zone of the North Atlantic.Limnol Oceanogr 35:464–471

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Editorial responsibility: Howard Browman (Associate Editor-in-Chief), Storebø, Norway

Submitted: January 12, 2007; Accepted: June 30, 2007Proofs received from author(s): November 28, 2007

primary production enhancement by artificial upwelling in a … · 2004 and 2005. pumping 2 m3...

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