Phytoplankton Dynamics in the Barents Sea Estimated from Chlorophyll Budget Models

Phytoplankton dynamics in the Barents Sea estimated from chlorophyll budget models

MARIA VERNET

Vernet, M. 1991: Phytoplankton dynamics in the Barents Sea estimated from chlorophyll hudgct models. Pp. 129-145 in Sakshaug. E., Hopkins, C. C. E. & Britsland. N. A. (cds.): Proceedings of the Pro Mare Symposium on Polar Marine Ecology, Trondheim, 12-16 May 1990. Polar Research lO(1). Pigment budgets use chlorophyll a and phaeopigment standing stock in combination with their photooxidation and sedimentation rates in the euphotic zone to estimate phytoplankton growth and grazmg by micro- and macrozooplankton. Using this approach. average phytoplankton growth in the euphotic zone of the Barents Sea was estimated at 0.17 and 0.14 d-' during spring of 1987 and 0.018 and 0.036 d-' during late- and postbloom conditions in bummer of 1988. Spring growth was 65% lower than the estimates from radiocarbon incorporation. supporting a 33% pigment loss during grazing. Macrozooplankton grazing and cell sinking were the main loss terms for phytoplankton during spring while microzooplankton grazing was dominant in summer. In contrast to tropical and temperate waters, Arctic waters are characterized by a high phaeopigment : chlorophyll a ratio in the seston. Photooxidation ratcs of phaeopigments at in situ temperatures (0 2 1°C) are lower than in temperate waters and vary by a factor of 2 for individual forms (0.009 to 0.018 m-* mol-'). The phaeopigment fraction in both the suspended and sedimenting material was composed of seven main compounds that were isolated using high-performance liquid chromatography and characterized by spectral analysis. The most abundant phaeopigment in the sediment traps, a phaeophorbide-like molecule of intermediate polarity ( phaeophorbide a,), peaked in abundance in the water column below the 1% isolume for PAR (6&80m) and showed the highest rate of photooxidation. This phaeopigment was least abundant in the scston when phytoplankton was dominated by prymnesiophytcs but increased its abundance in plankton dominated by diatoms. This distribution suggests that larger grazers feeding on diatoms are the main producers of this phaeopigment. Maria Vernet, Marine Research Division. Scripps Institution of Oceanography. University of California Sun Diego. La Jolla, California 92093-0218. USA.

1974; Hooks et al. 1988). Several forms of chloro- Introduction phyll a (Brown 1985; Chisholm et al. 1988) and Estimates of phytoplankton growth and fate of chlorophyll c (Jeffrey & Wright 1987; Nelson the newly formed carbon are essential to our & Wakeham 1989) in marine phytoplankton are understanding of the physical and biological pro- used as tracers of certain phyla. Fucoxanthin cesses that govern the distributions and trans- (Stauber & Jeffrey 1988), fucoxanthin derivatives formations of organic matter in an aquatic (Wright & Jeffrey 1987; Bjmnland et al. 1988), ecosystem. Due to its specificity to plants, chloro- and xanthophylls (Gieskes & Kraay 1983, 1986; phyll a has been successfully used as a tracer Guillard et al. 1985) are by themselves or in of phytoplankton carbon for the last 40 years combination with the chlorophylls also used as (Richards & Thompson 1952) and is one of the markers. Although not altogether quantitative, best estimators of phytoplankton abundance in this approach is complementary to other tech- marine waters. Chlorophyll a degradation prod- niques such as microscopy and can give a first ucts, in particular the fluorescent compounds, are approximation to the complexity and composition tracers of phytoplankton carbon in processes such of the phytoplankton assemblage. as grazing (Currie 1962), sedimentation (Lor- Chlorophyll degradation products are con- enzen et al. 1981; Bathmann & Liebezeit 1986), sidered quantitative estimators of grazing (Shu- and diagenesis in sediments (Daley & Brown man & Lorenzen 1975) and have been used in 1973; Hurley & Amstrong 1990). laboratory (Landry et al. 1984) and field studies Because of their specificity and abundance, (Welschmeyer et al. 1984; Downs & Lorenzen photosynthetic pigments have become important 1985) of herbivory activity. Based on premises tools in phytoplankton identification (Jeffrey of stoichiometric degradation of chlorophyll by 130 M. Vernet herbivory. Welschmeyer & Lorenzen (1985) stand the factors associated with this discrepancy. developed a pigment budget model to estimate In this study. phytoplankton growth and phytoplankton growth and losses. This model uses zooplankton grazing in the euphotic zone were chlorophyll a and phaeopigment standing stock estimated by a chlorophyll budget model. Dis- in combination with their photooxidation and tribution, sedimentation, and photooxidation sedimentation rates in the euphotic zone to esti- rates of phytoplankton pigments, in particular mate phytoplankton growth and grazing by micro- chlorophyll a and its degradation products, are and macrozooplankton. The model assumes that used as indicators of synthesis and transformation chlorophyll a is only associated with phyto- of organic carbon in the Barents Sea. When avail- plankton while phaeopigments are product of the able, the output of the pigment budget model is stoichiometric degradation of chlorophyll a due compared to other estimates in order to assess to grazing (or at least with a known loss fraction). the usefulness of this approach for Arctic waters. The usefulness of fluorescent degradation products as quantitative estimation of grazing has been challenged by a number of laboratory studies. Methods Klein et al. (1986), Conover et al. (1986) and Lopez et al. (1988) found high and variable (0- Samples for water column and sedimenting par- 99%) pigment losses in grazing experiments. In ticles were collected during two cruises to the contrast, field applications have found low (10- Western Barents Sea. The Pro Mare cruise 11 on 33%) losses (Dagg & Walser 1987; Downs 1989). R/V (3.0.SARS from 15 May to 12 June 1987 visited Laws et al. (1988), assuming a 33% pigment loss, 2 stations with 2 sediment trap deployments at found high correlation between growth rates esti- each station. Pro Mare cruise 15. on Norwegian mated from the pigment budget model and Coast Guard K/V ANDENES. from 1 to 21 July radiocarbon incorporation. It is clear that more 1988, visited 2 stations with one trap deployment experimentation is needed before we can under- at each station. Dates. positions, depth, and

I 80' N

70"

Fig. I. Water masses of the southwestern Barents Sea: open arrows = Atlantic 76' Water; striped arrow = Coastal Water; dashed arrows = Polar waters. Dotted line = position of Polar Front; shaded lines = average 74" position of ice edge during summer months as ice recedes northwards. Triangles indicate stations visited during spring 1987: open triangle = Stns. 72" 947-987; solid triangle = Stns. 941-994. Circles indicate stations visited during summer 1988: open circle = Stn. 864; 70 " solid circle = Stn. 885. NORWAY Redrawn from Rey & Loeng 2(1985). Phytoplankton dynamics in the Barents Sea 131

Table 1. Location, sediment trap sampling depth, and water column depth of 4 stations visited in the Barents Sea during this study. The spring bloom was underway in May-June 1987 while summer conditions prevailed in July of 1988.

Date Station Latitude Longitude Trap Water column depth depth (m) (m)

27 May-6 June 1987 937-947 75"00'N 28"37'E 50 320 2-7 June 1987 947-987 75"GQ'N 28"37'E 50 320 21-28 May 1987 894.941 74"29'N 31"31'E 50 230 28 May-8 June 1987 941-994 74"29'N 31"31'E 50 230 13-16 July 1988 864 73"OO'N 31"15'E 100 278 4-7 July 1988 885 75"OO'N 28"00'E 90 330

length of deployments are presented in Table 1 overnight at 4°C in the dark with 90% acetone. and Fig. 1. Extracts were cleared by filtration through What- Hydrographic profiles of temperature, con- man GF/C filters and injected onto the column ductivity and depth were obtained with a Neil without further treatment. Brown Mk 111 CTD-profiler mounted with a Gen- Pigments were estimated using the fluorometric eral Oceanic Rosette Sampler equipped with ten technique of Holm-Hansen et al. (1965) on a 10-1 Niskin bottles. The sampling depths were 0, Turner Designs fluorometer calibrated with 5, 10, 20, 30, 50, 75, 100, 150, 200 and 250111. chlorophyll a (Sigma Chemical Co.) in 90% Light was measured with a Photosynthetically acetone. This analysis was performed during both Active Radiation (PAR) 4n collector placed high cruises. In addition, samples for the summer on the ship superstructure (Biospherical Instru- cruise of 1988 were analyzed for chlorophyll a and ments model QSL-40). The extinction of light in degradation products ( phaeopigments) by high- the water column was estimated with a 4n PAR performance liquid chromatography (HPLC) on downwelling irradiance sensor (MER model a reverse-phase C-18 Brownlee Spherisorb ODS- 1012F optical profiling unit, Biospherical Instru- 5 column, 25 cm x 4.6 mm, 5 pm particles. Pig- ments Inc.). ments were eluted in a low-pressure gradient sys- Sedimentation was measured for a period of 3 tem consisting of a linear gradient from 100% A to to 11 days (see Table 1) using double cylindrical 100% B in 10 min and maintaining B for another PVC traps with a height of 1.6 m and a diameter 15min. Solvent A consisted of 70:20: 10 of 0.16 m (H/D ratio of 10). In May-June 1987, methanol : water: water + ion pairing agent (v/ traps were deployed at 50 and IOOm, while in v), the latter solvent in a concentration of 1.5 g July 1988 traps were deployed at 60, 100 and of tetrabutylammonium acetate and 0.96 g of 230m at Stn. 864 and at 40, 90, 150, 200 and ammonium acetate in 100 ml of water (Mantoura 250 m. No poisons were used during the deploy- & Llewellyn 1983). Solvent B consisted of 60:40 ments. The rate of carbon decomposition in the methanol :ethyl acetate (v/v). Eluting pigments sedimenting matter was, on average, not higher were quantified by fluorescence in a Hitachi F- than 2% d-l (Wassmann et al. 1991). The con- 3000 Fluorescence Spectrophotometer fitted with tents of each trap were transferred along with a flow-through cell, with excitation beam at about 2 liters. of seawater to a bottle and 410 nm and emission at 680 nm. Pigments were thoroughly mixed before subsampling. Triplicate identified by their fluorescence excitation spectra samples were taken and .filtered for pigments. (Table 2). The HPLC column was calibrated with Pigment sedimentation rates were calculated on pure pigments prepared as in Vernet & Lorenzen basis of the concentration in the trap, length of (1987) from a culture of Thalassiosira nor- the deployment, and trap surface area. denskioeldii, with extinction coefficients as in Samples were concentrated on Whatman GF/ Lorenzen & Downs (1986) for chlorophyll degra- F filters under 50 mbar of differential pressure. dation products, Jeffrey & Humphrey (1975) for Samples for high pressure liquid chromatography chlorophylls a and c~+~.Because of a lack of a (HPLC) were frozen in liquid N2 and stored at specific absorption coefficient, chlorophyll c3was -70°C until analysis. Pigments were extracted quantified using the same calibration as for 132 M. Vernet

Tuhle 2 Fluorescence maxima of pigmen15 analyaed b) reverse-phase high-performance liquid chromatography obtained from thcir fluorescence cxcitation \pectra Peak numbers as shwn in Fig 2 Spectra of the pigments were measured in the eluent in a Row-through cell attached to the 5pectrofluorometcr.

Peak Pigmcnc Retention FI uorescence number time (min) maxima (nm)

I C'hloroph\ll r dcribalivc hY 454. 585 Chlorophyllide o X 0 437. 624. bb5 3 Chloroph>ll c XY 450. 586,634 4 Phaeophorbidc a-like (a:) 95 425. 666 > Phaeophorbidc d-like (a,) 10.4 414. 614. 662 h Phaeophorbidr a-like (a,-<) 12.1 4OX. h24. 666 7 Chlorophyll Q + c derivatives 14.0 442. 462. 626. 667 X Chlorophyll u derivative 14.6 435. 624. 666 Chlorophyll u 15.0 435. 626. 667 I0 Phaeophytin a-like (a,) lY.5 117 5. 667 11 Phaeophytin a-like (al) 11.0 417 5, 666

chlorophylls c, even though a large error might depth of 1% incident radiation, defined as the be expected using this approach (Jeffrey & Wright depth of the euphotic zone. Pigment estimated 1987). by the Turner Designs fluorometer was used for Photooxidation estimates of phaeopigments this analysis because HPLC data for water column were obtained using material collected in the 100- phaeopigments were not available for June 1987. m traps in June 1987. Samples from the traps were diluted with filtered seawater. shaken to homogenize. and incubated in 250ml Pyrex bottles. Eight bottles were exposed to sunlight in Results an incubator placed on deck. Temperature was Hydrography. Spring conditions kept at 0 % 1°C with running seawater from the ship's water intake. One bottle was wrapped in Two stations were visited during the spring of aluminum foil and kept in the refrigerator. in the 1987 (Fig. 1). Stns. 947-987 were situated in dark. at 2"C, as control. The pigment content was Atlantic waters during a bloom of Phaeocystis measured at 3. 6. 12. 24. 36. and 48 hours of pouchetii. with chlorophyll a concentrations of 4 incubation. Photooxidation constants. k,. were to 6 mg m-3 from the surface to a depth of 60 to calculated as in Welschmeyer & Lorenzen (1985). 80 m. At this station stratification was very weak, Phytoplankton growth and zooplankton graz- nitrate was detectable through the mixed layer, ing were estimated from pigment budgets. In the and the euphotic zone (1% isolume PAR) summer cruise of 1988. steady state was assumed extended to 18 m (Wassmann et al. 1991). Stns. and the simplified equations presented in Welsch- 941-994 were located in an area under the influ- meyer & Lorenzen (1985) were used. Chlorophyll ence of the Polar Front (Rey & Loeng 1985) and sedimentation from the euphotic zone was not close to the ice edge. Stn. 941 was similar to Stn. assumed to be zero. and was estimated as C, C-', 947 but with only 1.3 mg chl a m-3 in the top 20 m where C, (mg chl a m-' d-I) is the chlorophyll of the water column. Ten days later, at Stn. 994, flux to the sediment traps and C (mg m-') is the a strong subsurface chlorophyll a maximum had integrated chlorophyll in the euphotic zone. In developed at 43-45m. at the depth of a strong the spring of 1987. during the bloom. equations halocline. due to surface meltwater. Nitrate was were solved numerically. including chlorophyll depleted in the mixed layer and the depth of 1%' sedimentation from the euphotic zone and isolume (PAR) was 41 m. Chlorophyll a con- accounting for changes in the depth of the centrations averaged 0.5 mg m-3 in the mixed euphotic zone as expressed in Laws et al. (1988). layer and peaked at 12 mg m-' at the maximum. Pigment concentration was integrated to the This temporal variability in the chlorophyll profile Phytoplatiktori dynmics in the Barents Sea 133 suggests strong advection in the area (Wassmann like pigments were found consistently in the water et al. 1990), precluding the use of the pigment column and sediment traps (Fig. 3). The budget model at this station. nomenclature corresponds to Vernet & Lorenzen (1987) also used by Downs (1989) and Hurley & Armstrong (1990). Two phaeopigments, not Summer conditions named in Vernet & Lorenzen (1987), less polar The stations visited in July 1988 were located in than phaeophorbide a3, were named a4 and a5, Atlantic waters (Fig. 1) and had already experi- as in Downs (1989). Phaeophorbide a5 was not enced &hespring bloom. Of the two, Stn. 885 had always well resolved from a4, the most abundant a deeper mixed layer (30 m), and a lower density of the two pigments (peak 6 in Fig. 3). Phaeo- gradient at the pycnocline (Wassmann et al. phytin al and a2 (peaks 10 and 11 in Fig. 3) were 1991). Nitrate concentrations were undetectable present in all samples. A third minor form eluted throughout the mixed layer and a nutricline was after al, but was not quantified. I present here established between 20 and 75 m. Chlorophyll a quantification of the more abundant phaeo- concentrations were 0.9mg m-3 in the mixed phorbide- and phaeophytin-like pigments, a2,a3 layer and had a subsurface maximum of 1.6mg and a4+5and a, and a,, respectively. nr3at the top the nutricline, at a depth of 30 m, with a secondary maximum at 60m (Fig. 2D). This station presents characteristics of late bloom Pigments in seston conditions in the Barents Sea when phytoplankton distribution changes from high con- The vertical profile of accessory chlorophylls fol- centration in the mixed layer to a deep chlorophyll lowed that of chlorophyll a (Fig. 2A and D). The maximum at the nutricline (Thingstad & Mar- abundance of chlorophylls c1+, and c3 at Station tinussen 1991 this volume). Station 864, further 885 during the late bloom suggests a dominance of north, had a shallower mixed layer (20 m) and a diatoms over prymnesiophytes (Jeffrey & Wright stronger density gradient than Stn. 885. Tem- 1987). The ratio of chlorophyll c3 :chlorophyll perature profiles revealed a warming of surface c1+2 (w/w) integrated over the top 100m was waters (5°C) over colder water (2.7"C). Nitrate 0.1. Stn. 864 was dominated by chlorophyll ci- concentrations were also undetectable at the containing algae, probably prymnesiophytes mixed layer. A nutricline was present from 50 to (Jeffrey & Wright 1987). The ratio of chl c3:chl 100m (Wassmann et al. 1991). Chlorophyll a cl+2(w/w) in the upper 100 m was 0.91. A ratio concentrations were low in the mixed layer of approximately 1.0 is commonly found in cul- (0.2 mg m-3) and peaked at about 75 m with a tures of prymnesiophytes, suggesting that most of concentration of 1.2 mg m-j at the depth of maxi- the chl c1+2is mostly c2 from the prymnesio- mum nutrient gradient (Fig. 2D). This station phytes. Deeper in the water column, at the depth represents summer, or postbloom, conditions in of the chlorophyll a maximum, chlorophyll c,+~ the Barents Sea (Thingstad & Martinussen 1991). become more abundant, suggesting more diatoms The euphotic zone, calculated as the depth of at the nutricline. 1% isoline for PAR, extended to 37 and 25m Vertical distribution of phaeopigments was for Stns. 864 and 885, respectively. While the similar to that of chlorophyll a. Maximum con- chlorophyll maximum during the late bloom was centrations coincided with the chlorophyll a maxi- at the bottom of the euphotic zone (Stn. 885), the mum at both stations although at Stn. 885 the chlorophyll maximum in the postbloom (Stn. 864) deep maximum (60m) was more conspicuous was well below the 1% isolume for PAR (Fig. than the shallow one (30 m). Phaeophorbide a4+5 2A and D). Although the exact position of the was the most abundant phaeopigment in the chlorophyll a maximum might have been lost due euphotic zone at both stations, followed by a2 and to low resolution in the sampling (depths sampled a,. Below the euphotic zone, the stations differed. were only 50,75 and 100 m), it was situated below At Stn. 885 phaeophorbides a3 and az became the 0.1% isolume for PAR (55 m). more abundant while phaeophorbide a4+5stayed dominant in the postbloom situation (Stn. 864). Phaeophytins presented a similar distribution to Phaeopigment diversity that of the phaeophorbides (Fig. 2C and F) but Five phaeophorbide-like and three phaeophytin- were more abundant during post-bloom con- 134 M. Vernet ditions (Stn. 864). Phaeophytin a, was generally similar pattern of both chlorophyll u and phaeo- more abundant than phaeophytin a,. pigments suggests that the chlorophyll a maximum at about 75 m was the main source of sedimenting matter at this station. Pigment sedimentation Sedimentation rates of phaeopigments showed The two stations in July of 1988 presented dif- different patterns among pigment forms and sta- ferent patterns of sedimentation for chlorophylls tions (Table 3). Phaeophorbide a3 was the most and phaeopigments (Table 3). Phaeopigment abundant degradation product in sediment traps. sedimentation (all forms of phaeophorbide and The only exception was at 60 m at Stn. 864 where phaeophytin combined) was always higher than phaeophorbide ad+5 showed the highest sedi- chlorophyll a sedimentation for any given depth mentation rate. Phaeophorbide a? had maximum sampled. During the late bloom (Stn. 885) chloro- sedimentation rates in the top 100 m during late- phyll a sedimentation was maximum at 40 and bloom conditions. with decreased sedimentation 90m and decreased at larger depths. Phae- rates with depth, while the opposite was observed opigment sedimentation was lower at 40m and in postbloom conditions (Stn. 864). Phaeo- was higher at 90m and deeper. At Stn. 864, phorbide u3had maximum rates of sedimentation during postbloom conditions, sedimentation of all at 90 or 100 rn. At greater depths, the pattern of pigments increased 5-fold from 60 to 100 m. The sedimentation differed for both stations. remain-

CI -E 5 so 8 0

100 0.00 0.03 0.06 0.09 0.12 0.15

~rr.di.nc~(EIn.1 mead")- Phbld. 2 I rgA) A-A-4 1.1 . -- 1.1.1. ..I,J 0.0 0.6 1.o 1 .s 2.0 0.00 0.03 0.06 0.09 0.12 0.16 Chl-. (rQA Phbld. 3 (Llg/l) tf. l.l.l''.j- 1.1.1.~.1, 0.0 0.6 1.o 1 .s 2.0 0.00 0.03 0.06 0.09 0.12 0.15 Chl-c (!Ae/l) Phb- 4+6 ( pa/l) 1.1." - - 0.0 0.6 1.o 1.s 2 .o Chl-CJ (rQ/l)

Fig. 2. Vertical profiles of pigments from 0 to 100 m at two stations in the Barents Sea visited during July 1988. Pigments were analysed by HPLC. lrradiance (thick line) is shown for each station in (A) and (D). Phytoplankton dynamics in the Barents Sea 135

0 0

25 25

I 1 E E CI u 5 50 g 50 a 0 a0 a

75 75

tY I ST.885 I

I,I,/,,, 100 100 0.00 0.02 0.04 0.06 0.08 0.10 0 2 4 6 8 10 Phytln 1 (up/I) A4-A Irradlanco (Elf181 m-*d-'I---

0.00 0.02 0.04 0.00 0.08 0.10 0.0 0.5 1.o 1.5 2.0 (pg/ll Chl-8 ( pgA) Phytln 2 tt. lII.l,I I 0.0 0.5 1.o 1.5 2.0 Chi-c ( pg/l) IIII1,I- I 0.0 0.5 1.o 1.5 2.0 0 Ch1-d ( pg/l) - 0

-E 25 I 5 50 8 - a E u 5 50 a e 75 0

75 \ 100 if I ' I*' I I 1 , I 0. > 0.09 0.06 0.00 0.12 0.15 Phblda 2 (pg/l) C-CI 1 L l,l,,,,,, 100 --- 0.00 0.03 0.06 0.09 0.12 0.15 0.00 0.02 0.04 0.06 0.08 0.10 Phbld. 9 (pg/I) tt. Phytln 1 (sg/l) I.IIl,I.I,l 0.00 0.03 0.06 0.00 0.12 0.15 0.00 0.02 0.04 0.06 0.08 0.10

PMd. 4+6 ( pa/l) Phytln 2 (pg/ll 0-0-0 136 M. Vernet

& Lorenzen (1985) are shown in Table 4. Phyto- plankton during the bloom of Phaeocystis pou- chrtii in Atlantic waters, not influenced by the Polar Front, grows at an average rate in the euphotic zone of 0.14-0.17 d-'. Macrozooplank- ton grazing (0.054.06 d-') dominated over microzooplankton grazing (0.01-0.02 d- I), accounting for approximately 35% of the phytoplankton loss. Sinking of intact cells out of the euphotic zone. estimated from the sedimentation rate of chlorophyll a, was 7-8% of the growth. Between 45 to 50% of the newly formed chloro- 5 10 15 20 25 phyll accumulated in the euphotic zone. When TIME (rnin) compared to growth rates estimated from I4C Fig. 3. Chromatogram zhouing chloroph>ll a and chlorophyll incorporation, assuming a C : chla ratio of 75 from degradation products from 3 5edirnent trap sample collected in the POC data (F. Rey, unpubl. data) and growth July 1988 in the Barents Sea Pigments were analyscd with a calculations according to Eppley (1972), the reverse-phase HPLC and detected by Ruorcscence with exci- model underestimated phytoplankton growth by tation wave length at 42Onrn and emission at 680nm. Peak 35%. Due to the lack of independent estimates identities correspond to those in Table ?. of the phytoplankton C:chla ratio, it is not possible to determine how much pigment might have been lost during grazing (i.e. Lopez et al. 1988). ing high at Stn. 885 while decreasing at Stn. 864. A loss of 33% though is expected during macro- Phaeophorbide a.,, increased their sedimen- lankton grazing (Downs 1989) and seems to be a tation rates with depth. with the exception of representative pigment loss term in the spring 100m at Stn. 864 where rates peaked. Sedi- bloom (Laws et al. 1988). mentation rates of phaeophytin a?,the form least Estimates of phytoplankton growth rates for abundant in the water column. were always equal the summer were an order of magnitude lower to or larger than those of phaeophytin a,. The than for spring (Table 4). Macrozooplankton pattern of sedimentation of the 2 phaeophytins grazing rates were also an order of magnitude was similar to that of phaeophorbide ~2.In lower than in the spring. while microzooplankton general, maximum rates of sedimentation were grazing rates were about the same. In late bloom found at 90 and 100 rn at Stns. 864 and 885 respect- conditions (Stn. 885), where diatoms dominated ively, immediately below the depth of the pigment in the water column, micro- and macrozooplank- maxima, where diatoms were more abundant. ton grazing were comparable. Ten percent of the chlorophyll sank out of the euphotic zone and about 8% still accumulated. In postbloom con- Phaeopigment photoxidation rates ditions, where small flagellates were dominant, The results from the 3 experiments were com- microzooplankton grazing accounted for 85% of bined and the resultant first order photooxidation the phytoplankton growth, while 7% sank out of decay constant, k, (m? mol-I) was computed. the euphotic zone, and there was almost no net Photooxidation rate constants vary among the accumulation of phytoplankton in the euphotic individual chlorophyll degradation forms by a zone. No radiocarbon incorporation data are factor of 2. from 0.009 to 0.015 m' mol-l (Fig. 4). available from this cruise in order to compare The average photooxidation rate constant for all growth estimates. pigment combined (SUM PHAEO) was 0.012 m' mol-'. Discussion Pigment model Arctic phytoplankton The estimations of phytoplankton growth rate and zooplankton grazing during spring and sum- Phytoplankton growth at the ice edge of polar mer based on the pigment model of Welschmeyer regions is characterized by an intense growth Phytoplankton dynamics in the Barents Sea 137

Table 3. Biomass and sedimentation rates of chlorophyll a and its main degradation products during July 1988. Pigments were analysed and quantified by HPLC. Pigment identification as in Table 2 and Fig. 2. "Sum Phaco" dcnotcs total phacopigment. Pigment biomass was integrated from the surface to the depth of the euphotic zone. Scdinicntation rates were calculated without correction for daily losses, estimated to be <2% d-' (Wassmann et al. 1991). Pcrcentage loss wa5 estimated as (sedimentation x 100/biomass) in units of d-'.

Station Pigments

864 Phbide 2 60 0.45 0.1 0.22 Phbide 3 0.42 0.3 0.71 Phbide 4 + 5 0.90 1.2 1.33 Chi a 13.67 2.5 0.18 Phytin 1 0.86 0.2 0.23 Phytin 2 0.48 0.2 0.42 Sum Phaeo 3.11 2.0 0.64 Phbide 2 I00 I .29 2.0 I .55 Phbide 3 2.85 24.3 8.53 Phbide 4 + 5 4 09 7.0 1.71 Chl a 54.83 15.9 0.29 Phytin 1 2.83 2.5 0.88 Phytin 2 2.22 4.5 2.03 Sum Phaeo 13.28 40.3 303.0 Phbide 2 230 1.29 1 .x 1.40 Phbide 3 2.85 5.8 2.04 Phbide 4 + 5 4.09 4.0 0.98 Chl a 54.83 2.5 0.05 Phytin 1 2.83 1.1 0.39 Phvtin 2 2.22 I .4 0.63 Sum Phaeo 13.28 21.7 163.0 885 Phbide 2 40 0.94 1.7 181 Phhide 3 0.71 5.5 7.75 Phbide 4 + 5 I 39 3.2 2.01 Chl a 38.11 7.2 0.19 Phytin 1 0.97 0.8 0.82 Phytin 2 0.87 1.7 1.95 Sum Phaeo 5.08 12.9 253.0 Phbide 2 90 3.01 1.8 0.60 Phbide 3 3.20 14.9 4.66 Phbide 4 + 5 3.08 3.9 1.27 Chl a 47.9 6.8 0. I4 Phytin I 1.95 1.5 0.77 Phytin 2 1.66 3.8 2.29 Sum Phaeo 12.99 25.Y 109.0 Phbide 2 150 3.01 1 .0 0.33 Phbide 3 3.20 13.9 4.34 Phbide 4 + 5 3.08 6.0 1.95 Chl a 47.95 2.9 0.06 Phytin 1 1.95 1.1 0.56 Phytin 2 1.66 1 .9 1.14 Sum Phaco 12.99 23.9 184.0 Phbide 2 200 3.01 I .0 0.33 Phbidc 3 3.20 17.6 5.50 Phbide 4 + 5 3.08 7.8 2.53 Chl a 47.95 2.3 0.05 Phytin I I .95 0.8 0.41 Phvtin 2 1.66 1.4 0.84 Sum Phaco 12.95, 28.6 220.0 Phbide 2 250 3.01 0.7 0.23 Phbide 3 3.20 15.3 4.78 Phbide 4 + 5 3.08 7.2 2.34 Chl a 47.95 2.5 0.05 Phytin 1 1.95 0.9 0.46 Phytin 2 I .66 1.1 0.66 Sum Phaeo 12.99 25.2 194.0 138 M. Verne1

Phbide 3 O.OOt .. A

0 a 3

Rz= 085 a=431 -3 00 0 40 80 120 1 i0 (rn2Eins.t -l )

Phbide 4 Phytin 1 O.00t . O.OOt* . 1

a .I e J J k = 401 R’= 069 a = 0083 Fig. 4. Estimation of -3 00 -300 0 40 80 120 160 0 40 80 120 160 photooxidation rate constants (rn2Einst.1 ) (rn2Einst-’ ) for the chlorophyll degradation products abundant in the water column Phytin 2 SUM PHAEO and sediment trap matter. o.00T = I 0.00 Data include three experiments incubated on deck in June 1987 from hm El material collected in 100-m - -1.00 traps at Stns. 941-994 and 0 947-987. Temperature was maintained at 0 ? 1°C with running seawater from the ship’s intake. Peak 4 is a R2= 049 mixture of phaeophorbide a = 431 a= a.z? (I,+%. SUM PHAEO (F) is the -3.00 -. .,- average photooxidation rate 0 40 80 120 160 0 40 80 120 Is0 constant for all the (m2Einst -l ) (m‘Einst -‘) phaeopigments combined.

period during the spring due to increased sta- either due to ice melting at the ice edge or to bilization of the water column. sun angle and warming of surface layers, as in the case of Atlan- daylength (Dunbar 1981; Rey et al. 1987; Nie- tic waters in the southwestern area of the Barents bauer & Alexander 1989; Sakshaug 1989). In the Sea (Skjoldal et al. 1987; Loeng 1989). Winter Arctic, and in particular in the northern part of and summer are generally dominated by small the Barents Sea, the bloom crashes after nitrate flagellates while spring blooms are due to either has been stripped from the mixed layer and marks diatoms and/or Phaeocystis poucherii (Rey et al. the onset of the summer period which is charac- 1987). While diatoms are generally present in the terized by a subsurface chlorophyll a maximum Atlantic waters of the Barents Sea, P. pouchetii near the nutricline. The stratification of water is is dominant in ice edge blooms (Wassmann et al. Phytoplankton dynamics in the Barents Sea 139

Table 4. Results from pigment model as in Wclschmeyer & Lorenzen (1985). Stations durmg May/June 1987 wcrc solved numcrically. accounting for changes in mixed layer depth and accumulation of biomass in thc euphotic zonc, 3s in Laws ct al. (1988). Stations in July 1988 were assumed to be in steady state and solved as in Wclschmeyer & Lorcnzen (1985). Primary production measurements were used to estimate phytoplankton growth rate according to Epplcy (1972) and using thc Carbon: chlorophyll ratio estimated from particulate (POC) data*. Stations 896/911/994 in May/June 1987 wcrc not considcrcd due to lateral advection present at the stations. Macro and micro refer to macrozooplankton and microzooplankton; sinking is an estimate of sinking rate of intact cells as indicated by the scdimcntation rate of chlorophyll a, accum refers to the fraction of phytoplankton growth that remains in the euphotic zonc.

Station Zooplankton Phytoplankton Mass balance *Phytoplankton grazing growth growth (d-') (d-') (d-')

Macro Micro Macro Micro Sinking Accum

July 1988 864 0.0024 0.0309 0.036 7% 85% 7%' 1% - 885 0.0059 0.0087 0.018 33% 49% 10% 89% - May 1987 947 (11) 0.06 0.02 0.17 34% 13% 8% 45% 0.2 987 (12) 0.05 0.01 0.14 36% 7% 7% 50% 018

1990), either after a diatom bloom, when silicate and the density stratification is weak. On the becomes limiting for diatoms, or from the onset other hand, small flagellates characterize deep or of the bloom. Similar observations have been nutrient-depleted mixed layers, encountered in made in the Greenland Sea (Cota et al. 1990) either pre- or postbloom conditions. In this study, and in the waters around Iceland (Stefansson & large diatoms were abundant in late spring (Stn. Olafsson 1990). 885) but were displaced by prymnesiophytes in Diatoms were dominant in the blooms of Atlan- the mixed layer as nitrogen became low. These tic waters in June of 1987 (Vernet unpubl. data) diatoms still grew at the depth of chlorophyll and during late-bloom conditions in July of 1988 maximum in summer conditions (Stn. 864), when (Stn. 885). Single cell prymnesiophytes (i.e. Emi- irradiance was low but rates of nutrient supply liana huxleyi) were present in pre-bloom con- were probably high. This scenario supports the ditions in May 1987 (Vernet unpubl. data) and hypothesis that large cells can grow in environ- increasingly dominant from late-bloom to post- ments where there is an increase in the rate of bloom in July 1988 (Stn. 864). At the ice edge in nutrient supply (Thingstad & Sakshaug 1990). May-June 1987, more than 95% of the plankton consisted of P. pouchetii cells (C. Hewes, pers. Chlorophyll degradation comm.). The distribution of accessory pigments gave a good approximation to characterizing these The more abundant forms of chlorophyll a degra- phytoplankton assemblages in the Barents Sea dation found in seston and sedimenting particles (Fig. 2). Plankton dominated by diatoms were of the Barents Sea (see Fig. 2) are similar to the rich in chl c,+~(Stauber & Jeffrey 1988), while forms found in temperate coastal marine waters those with prymnesiophytes such as E. huxleyi (Klein & Sournia 1987; Vernet & Lorenzen 1987; and P. pouchetii had chl c3 in addition to chl c2 Downs 1989; Roy & Poulet 1990), lakes (Car- (Jeffrey & Wright 1987). With respect to carpenter et al. 1986; Hurley & Armstrong 1990) and otenoids, E. huxleyi has 19' hexanoyloxyfu- sediments (Brown et al. 1977). The uniformity of coxanthin as the main carotenoid (Vernet 1989). components suggests common catabolic pathways Diatoms and P. pouchetii have focuxanthin in aquatic environments (Hendry et al. 1987). In (Wassmann et al. 1990). The difference in dom- Arctic waters, as in other areas of the ocean, the inant carotenoid within the prymnesiophytes main pathways of chlorophyll degradation involve makes it possible to differentiate them. biotic and abiotic factors. Oxidizing and non- Large cells such as diatoms and the colonial oxidizing enzymes from either the alga itself or a form of P. pouchetii dominate the spring bloom, grazer that has ingested it, light, bacterial activity, at which time there are shallow mixed layers, and oxygen are the main degradative agents nitrate is present in measurable concentrations, (Hendry et al. 1987). The last two sources can be 140 M. Veriier considered secondary in short periods of time can be calculated as the decay rate of the corn- (Downs 1989; Roy & Poulet 1990). particularly bined pigments (Fig. 4F). For a more accurate in polar waters (Wassmann et al. 1991). In the calculation of the photooxidation rate of the euphotic zone, light plays a main role in the whole phaeopigment assemblage we should degradation of chlorophyll and phaeopigments include the relative contribution of each indi- associated to detritus. Pigments are degraded to vidual component. colorless compounds (Struck et al. 1990). the Photooxidation rates measured in this study at main product of photooxidation (SooHoo & Kie- 0°C are lower than previously published data for fer 1982; Welschmeyer & Lorenzen 1985; Vernet temperate waters (SooHoo & Kiefer 1982; & Lorenzen 1987; Downs 1989). In the absence of Welschmeyer & Lorenzen 1985; Downs 1989) and light, below the euphotic zone. enzymatic activity support the hypothesis of temperature depen- resulting from zooplankton grazing may be the dence. Welschmeyer & Lorenzen (1985) and main factor of chlorophyll degradation. Activity Downs (1989) found photooxidation rates to be from cellular enzymes. such as chlorophyllase. independent of temperature. The authors suggest dephytylizes chlorophyll a in diatoms (Jeffrey & that the source and type of phaeopigment are a Hallegraeff 1987). From chlorophyllide further probable cause of the variability observed. The enzymatic activity has been found to produce rates measured in this study suggest otherwise. pyropheophorbide via phaeophorbide in cultures Individual rates of phaeopigments measured by of Chlorella fusca. Pyrophaeophorbide. the end HPLC and the combined photooxidation constant product, was found to be very stable in the dark show lower degradation rates at lower tem- and thus accumulated (Ziegler et al. 1988). It is peratures. Fig. 5 shows an Arrhenius plot includ- clear that further studies are needed in order to ing all the published k, values from marine characterize the different forms of phaeophorb- environments where temperature has been ide-like molecules and other degradative forms measured. They have been converted to units of (Matile et al. 1989). The constancy of the mol- m' mol-' (Table 5). The regression obtained is ecules analyzed, common to so many environ- similar to the one by SooHoo & Kiefer (1982). ments, justify the effort. About 35% of the variance is still unexplained Photooxidation rates of chlorophyll degr2.- suggesting that other variables, such as type of dation seem to follow first-order kinetics (SooHoo light sensor, type of dominant form of phae- & Kiefer 1982; Welschmeyer & Lorenzen 1985). opigment, calibration of the fluorometer, incident At O'C, photooxidation rates of individual phaeopigments vary by a factor of 2 (Fig. 4A-D). In the Barents Sea. phaeophorbide a3 had the highest rate of photooxidation, followed by phaeophorbide a! and phaeophorbide a,. The lowest rates are associated with the less polar forms, phaeophorbides a,,,. Both forms of phaeophytins also had lower rates than the more polar phaeophorbides. Downs (1989) found the same differences among phaeophorbides a2 and a3, although the constants were, on the average. 3 to 5 times higher. An important corollary of a=477 the difference in photooxidation rates of r2= 0% ~ phaeopigments is that the distribution of rn I

0.01 + phaeopigments in the euphotic zone has to be 3.3 3.4 , 3.5 3.6 3.7 - 10 -3(aK-1) interpreted in light of these differences. where the T abundance is a function of the balance between FIR.5. Arrhenlus plot of the photooxidation rate constant as a production and loss rates. Distributions depicted function of temperature. Estimates from marine waters have in Fig. 2 and photooxidation rates in Fig. 4 suggest hcen pooled: (solid squarc) SooHoo & Kicfer (19x2): (cross) that phaeophorbide a,, can accumulate twice as Wclschrncyer & Lorenzen (1985): (open square) Downs (19x9): (triangle) Vcrnct & Mitchell (19YU): (asterisk) this study. Tem- fast as phaeophorbide a3for a similar production perature range from -0" to 28°C (see Table 4). Statistics and rate. and may account in part for their abundance \driancc cxplaincd arc similar to those ohtaincd by SooHoo & in the euphotic zone. Total photooxidation rate Kicfcr (19x2). Phytoplankton dynaniics in the Barerits Sea 131

Table 5. Summary of the first order photooxidation decay constant of phaeopigmcnts

~~~ ~ Source k,. 10.' Substratc Temperature (m'/Einst)

~ ~ SooHoo & Kiefcr (1982) 1.1-8.8 Scston fecal pcllcts &28T Welschmeyer & Lorcnzcn (1985) 6.75 Scston -Y-?VC Barents Sea (this study) 1.20 Sediment trap -1-+2"C Vernet & Mitchell (1990) 1.87 Scdiment trap - 1-+2"C Downs (1989) 3.693.9 Scdimcnt trap 1+21"C

spectral irradiance, and probably size of the par- plankton present. Phaeophorbide was more ticles containing phaeopigments, can introduce abundant in the station dominated by prym- uncertainty in this type of measurement. The nesiophytes while phaeophorbide a3 was pro- lack of a significant temperature dependence in duced by degradation of diatoms. It is not possible photooxidation rates in Welschmeyer and to differentiate with the present sampling design Lorenzen (1985) and Downs (1989) studies may if the degradation is originated by enzymes in the be due to the narrower range of temperatures phytoplankton or in the grazers if we assume a studied and the logarithmic relationship between close coupling between phytoplankton groups and these 2 variables. types of grazers. The dominant form of phaeo- Accurate values of photooxidation rate con- phorbide related to the pair alga-grazer is present stants become increasingly important at lower not only in the seston but also in the large particles temperatures. A sensitivity analysis showed that that sink out of the surface and are caught by the the total contribution of microzooplankton graz- sediment traps. If, as hypothesized by Shuman ing to total grazing in the pigment model (1978) and Welschmeyer & Lorenzen (1985), decreases rapidly at lower values of k, (Fig. 6). phaeopigments in the seston are mainly due to The model is then most sensitive for low photo- microzooplankton grazing while sinking faecal oxidation rate constants, in the range of values pellets originate mainly from macrozooplankton, measured for Arctic waters. the dominance of the same phaeopigment Specific forms of chlorophyll degradation seem both in the water column and sediment trap sug- to be quantitatively related to the type of phyto- gest that the pathway of chlorophyll degradation is related more to the alga than to the grazer. Sedimentation of the most abundant phaeophorbide a in lakes was due to the presence of large grazers (Laevitt & Carpenter 1990) pre- sumably feeding on large algae.

Pigment sedimentation Pigment sediment out of the euphotic zone by either direct sinking of phytoplankton cells, phy- 0.21 todetritus, or through zooplankton fecal pellets. Intact phytoplankton cells contain almost exclus- ively non-degraded chlorophyll a pigments while 8.100 ' 0.02 ' 0.04 ' 0.06 ' 0.08 ' 0.iO k,(m2 Einst-') the pigments of faecal pellets are mostly phaeo- Fig. 6. Temperature dependence of photooxidation ratc con- pigments (but see Wassmann et al. 1990). Never- stant in the pigment budget model (Welschmcyeer & Lorenzen theless some undegraded chlorophyll a in the 1985): scnsitivity analysis of the contribution of micro- sediment traps could originate from faecal pellets zooplankton grazing (g) to total grazing (g + g') as a functlon (Vernet & Lorenzen 1987). In this way, estimates of the photooxidation rate constant (k,), Arrows indicatc three photooxidation ratc constants: this study (0.012 m2Einst-'). of cell sinking based on chlorophyll a sedi- SooHoo & Kiefer (1982) (0.037 m'Einst-') and Wclschmeycr mentation rates would be maximum. & Lorenzen (0.0675 m?Einst-'). Maximum sedimentation rates of phaeopig- 142 M. Vernet ment measured below the chlorophyll maximum plankton growth rate estimates for summer sta- at both stations suggest that most of the defecation tions at the Barents Sea (Stns. 864 and 885) are of pigments occurred while zooplankton were lower than might be expected for phytoplankton feeding at the chlorophyll maximum, as shown by growing at high irradiance in stratified waters. Welschmeyer et al. (1984) and Dagg et al. (1989) Growth rates estimated from primary production in coastal areas. If the active transport of pigments measured in the same area in June-July 1979 by zooplankton to depth through vertical (Ellertsen et al. 1982). and assuming a C:chla migration is minimum (Dagg et al. 1989), sedi- ratio of 100. are in the order of 0.064.1 d-l, 2 to mentation rates at depth are dependent mostly of 10 times higher than the estimated rates (Table the remineralization or reingestion of pigments by 4). Similar discrepancies are observed in tropical other plankton at mid-depth. The higher changes environments. Laws et al. (1988) suggest that observed from 100 to 230 m at Stn. 864 suggest phytoplankton growth rates in the Central Pacific higher recycling of sinking organic matter in the might be underestimated by 6670 if we compare summer with respect to late spring (from 90 m to data from the pigment model (Welschmeyer & 250m at Stn. 885). The constant sedimentation Lorenzen 1985) to the direct measurements of rate of pigments below 150m at both stations growth rate (Laws et al. 1987). Both tropical and (except phaeophorbide a3)indicate that most of Arctic data indicate that where nutrient recycling the transformation may occur immediately below is important and where small algae and small the maximum pigment flux. grazers are dominant, there is a higher loss factor Although all forms of phaeopigment were in the conversion of chlorophyll to phaeopig- found at all stations, there seems to be a quan- ments. An alternative scenario could be that the titative relationship between some phaeo- observed phaeopigment :chlorophyll ratio would phorbides and the type of phytoplankton. Phaeo- be averaged over a longer food web each of them phorbide a3, with high and constant sedi- with a 35% loss in each step of the food web. mentation rates below 100111, seems to be Independent of the reason, summer situations in associated to large particles that sink fast and are the Arctic seem more similar to tropical stations not recycled at mid depths. These results agree with an average conversion factor larger than with higher presence of this pigment in seston 66%. These results are thus in agreement with associated with larger cells, i.e. diatoms, at the studies where pigments were useful tracers of chlorophyll a maxima at both stations. Phae- macrozooplankton grazing (Dagg et al. 1987) ophorbide a,,+ is proportionally more abundant while the opposite is true for microzooplankton where prymnesiophytes dominate, at Stn. 864, (Klein et al. 1986; Strom 1988). but it is also related to fast sinking particles, During the spring bloom, phytoplankton grew particularly at Stn. 885. In general, mid-water at maximum growth rates for the ambient light recycling seems to be more important at Stn. 864. and temperature present at that time of year. during summer conditions, although a lack of Growth rate estimates of 0.14-0.17 d-l in 1987 sampling at intermediate depths makes these con- were calculated based on a mean irradiance in the clusions tentative. euphotic zone of 1.6611101 m-' d-'. Planktonic diatoms isolated from the Barents Sea, grown at 18 pmol m-2 SKIof continuous light (total daily Phytoplankton population dynamics mean irradiance of 1.55mol m-* d-l), had an The rate of phytoplankton growth estimated by average growth rate of 0.17 d-' (Gilstad & Sak- the pigment budget model during the spring (Stns. shaug 1990), in good agreement with the model 947 and 987) is about 65% of the estimate using estimates. radiocarbon incorporation. These numbers are In conclusion, estimates of phytoplankton within what is expected if we assume a pigment dynamics based on chlorophyll budgets can be conversion efficiency of about 65% from a large used with reliability during ice edge blooms of phytoplankton to a large grazer (Shuman & Lor- Arctic waters. During summer conditions the enzen 1975; Welschmeyer & Lorenzen 1985; model seems to underestimate phytoplankton Laws et al. 1988; Downs 1989). These numbers growth. Mass balances of C are within expected seem to indicate that chlorophyll budgets are values during both seasons, although the mag- good indicators of phytoplankton dynamics dur- nitude of any given pool must be underestimated ing spring bloom. On the other hand, phyto- during the summer. The model parameters used Phytoplankton dynamics in the Barents Sea 143

for temperate and tropical waters cannot be terization of lacustrine chlorophyll diagenesis. I. Physio- directly applied to polar areas, in particular the logical and environmental effects. Arch. Hvdrobiol. 72. 277- photooxidation rate constant for phaeopigments. 304. Downs, J. N. & Lorenzen, C. J. 1985: Carhon:pheopigment A close look at the individual phaeopigments in ratios of zooplankton fecal pellets as an index of herbivorous the water column and sedimenting matter can feeding. Limnol. Oceanogr. 30, 102C1036. give insight into phytoplankton-grazer inter- Downs. J. N. 1989: Implications of the phaeopigment. carbon actions. Furthermore, information on phyto- and nitrogen content of sinking particles for the origin of plankton composition based on distribution and export production. Ph.D. Thesis, Univ. Washington, Seattle. 197 pp. abundance of accessory pigments can relate graz- Dunbar, M. H. 1981: Physical causes and biological significance ing to food availability. of polynyas and other open water in sea ice. Pp. 29-35 in Stirling, 1. & Cleater, H. (eds.): Polynyas in the Canadian Acknowledgements. - I thank P. Wassmann for the sediment Arctic. Occm. Pap. 45. Can. Wild. Serv. trap samples, F. Rey for primary productivity data. H.-R. Eilertsen, F., Hassel, A,, Loeng. H.. Rey, F.. Tjelmeland. S. Skjoldalfor shiptime, G.Johnsen for HPLC analyses, E. Brody & Slagstad, D. 1982: Bkologiske undersokelser nm iskanten for data analysis and graphics, E. Sakshaug for financial support, i Barentshavet somrene 1979 og 1980. Fisken og Hauet (1982) and E. Sakshaug, P. Wassmann and B. G. Mitchell for critical 3, 31-83. review of the manuscript. This study was supported by NSF Eppley, R. W. 1972: Temperature and phytoplankton growth grant DPP-8520848 and by the Norwegian Research Council in the sea. Fish. Bull. U.S. 70, 10631085. for Science and Humanities (NAVF). Gieskes, W. W. 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