Phytoplankton dynamics in the Barents Sea estimated from chlorophyll budget models MARIA VERNET Vernet, M. 1991: Phytoplankton dynamics i n the Barents Sea estimated from chlorophyll hudgct models. Pp. 129-145 i n 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 photo- oxidation 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 3 3 % 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 tem- peratures (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 phaeo- phorbide-like molecule of intermediate polarity ( phaeophorbide a , ) , peaked i n 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 i n 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. Introduction Estimates of phytoplankton growth and fate of the newly formed carbon are essential to our understanding of the physical and biological pro- cesses that govern the distributions and trans- formations of organic matter in an aquatic ecosystem. Due to its specificity to plants, chloro- phyll a has been successfully used as a tracer of phytoplankton carbon for the last 40 years (Richards & Thompson 1952) and is one of the best estimators of phytoplankton abundance in marine waters. Chlorophyll a degradation prod- ucts, in particular the fluorescent compounds, are tracers of phytoplankton carbon in processes such as grazing (Currie 1962), sedimentation (Lor- enzen et al. 1981; Bathmann & Liebezeit 1986), and diagenesis in sediments (Daley & Brown 1973; Hurley & Amstrong 1990). Because of their specificity and abundance, photosynthetic pigments have become important tools in phytoplankton identification (Jeffrey 1974; Hooks et al. 1988). Several forms of chloro- phyll a (Brown 1985; Chisholm et al. 1988) and chlorophyll c (Jeffrey & Wright 1987; Nelson & Wakeham 1989) in marine phytoplankton are used as tracers of certain phyla. Fucoxanthin (Stauber & Jeffrey 1988), fucoxanthin derivatives (Wright & Jeffrey 1987; Bjmnland et al. 1988), and xanthophylls (Gieskes & Kraay 1983, 1986; Guillard et al. 1985) are b y themselves or in combination with the chlorophylls also used as markers. Although not altogether quantitative, this approach is complementary to other tech- niques such as microscopy and can give a first approximation to the complexity and composition of the phytoplankton assemblage. Chlorophyll degradation products are con- sidered quantitative estimators of grazing (Shu- man & Lorenzen 1975) and have been used in laboratory (Landry et al. 1984) and field studies (Welschmeyer et al. 1984; Downs & Lorenzen 1985) of herbivory activity. Based on premises of stoichiometric degradation of chlorophyll by 130 M. Vernet herbivory. Welschmeyer & Lorenzen (1985) developed a pigment budget model t o estimate phytoplankton growth and losses. This model uses chlorophyll a and phaeopigment standing stock in combination with their photooxidation and sedimentation rates in the euphotic zone t o esti- mate phytoplankton growth and grazing by micro- and macrozooplankton. T h e model assumes that chlorophyll a is only associated with phyto- plankton while phaeopigments a r e product of the stoichiometric degradation of chlorophyll a d u e to grazing (or at least with a known loss fraction). The usefulness of fluorescent degradation prod- ucts as quantitative estimation of grazing has been challenged by a number of laboratory studies. Klein e t al. (1986), Conover e t al. (1986) and Lopez et al. (1988) found high and variable (0- 99%) pigment losses in grazing experiments. In contrast, field applications have found low (10- 33%) losses (Dagg & Walser 1987; Downs 1989). Laws et al. (1988), assuming a 33% pigment loss, found high correlation between growth rates esti- mated from t h e pigment budget model and radiocarbon incorporation. It is clear that more experimentation is needed before we can under- I 80' N 70" 76' 74" 72" 70 " stand the factors associated with this discrepancy. In this study. phytoplankton growth and zooplankton grazing in t h e euphotic zone were estimated by a chlorophyll budget model. Dis- tribution, sedimentation, and photooxidation rates of phytoplankton pigments, in particular chlorophyll a and its degradation products, are used as indicators of synthesis and transformation of organic carbon in t h e Barents Sea. When avail- able, the output of t h e pigment budget model is compared t o other estimates in order to assess the usefulness of this approach for Arctic waters. Methods Samples for water column and sedimenting par- ticles were collected during two cruises to the Western Barents Sea. T h e Pro Mare cruise 11 o n R/V (3.0. SARS from 15 May to 12 J u n e 1987 visited 2 stations with 2 sediment t r a p deployments at each station. Pro Mare cruise 15. o n Norwegian Coast G u a r d K / V ANDENES. from 1 t o 21 July 1988, visited 2 stations with o n e t r a p deployment at each station. Dates. positions, depth, and 2 NORWAY Fig. I . Water masses of the southwestern Barents Sea: open arrows = Atlantic Water; striped arrow = Coastal Water; dashed arrows = Polar waters. Dotted line = position of Polar Front; shaded lines = average position of ice edge during summer months as ice recedes northwards. Triangles indicate stations visited during spring 1987: open triangle = Stns. 947-987; solid triangle = Stns. 941-994. Circles indicate stations visited during summer 1988: open circle = Stn. 864; solid circle = Stn. 885. Redrawn from Rey & Loeng (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 and Fig. 1. Hydrographic profiles of temperature, con- ductivity and depth were obtained with a Neil Brown Mk 111 CTD-profiler mounted with a Gen- eral Oceanic Rosette Sampler equipped with ten 10-1 Niskin bottles. The sampling depths were 0, 5 , 10, 20, 30, 50, 75, 100, 150, 200 and 250111. Light was measured with a Photosynthetically Active Radiation (PAR) 4 n collector placed high on the ship superstructure (Biospherical Instru- ments model QSL-40). The extinction of light in the water column was estimated with a 4 n PAR downwelling irradiance sensor (MER model 1012F optical profiling unit, Biospherical Instru- ments Inc.). Sedimentation was measured for a period of 3 to 11 days (see Table 1) using double cylindrical PVC traps with a height of 1.6 m and a diameter of 0.16 m (H/D ratio of 10). In May-June 1987, traps were deployed at 50 and IOOm, while in July 1988 traps were deployed at 60, 100 and 230m at Stn. 864 and at 40, 90, 150, 200 and 250 m. No poisons were used during the deploy- ments. The rate of carbon decomposition in the sedimenting matter was, on average, not higher than 2% d-l (Wassmann et al. 1991). The con- tents of each trap were transferred along with about 2 liters. of seawater to a bottle and thoroughly mixed before subsampling. Triplicate samples were taken and .filtered for pigments. Pigment sedimentation rates were calculated on basis of the concentration in the trap, length of the deployment, and trap surface area. Samples were concentrated on Whatman GF/ F filters under 50 mbar of differential pressure. Samples for high pressure liquid chromatography (HPLC) were frozen in liquid N 2 and stored at -70°C until analysis. Pigments were extracted overnight at 4°C in the dark with 90% acetone. Extracts were cleared by filtration through What- man GF/C filters and injected onto the column without further treatment. Pigments were estimated using the fluorometric technique of Holm-Hansen et al. (1965) on a Turner Designs fluorometer calibrated with chlorophyll a (Sigma Chemical Co.) in 90% acetone. This analysis was performed during both cruises. In addition, samples for the summer cruise of 1988 were analyzed for chlorophyll a and degradation products ( phaeopigments) by high- performance liquid chromatography (HPLC) on a reverse-phase C-18 Brownlee Spherisorb ODS- 5 column, 25 cm x 4.6 mm, 5 pm particles. Pig- ments were eluted in a low-pressure gradient sys- tem consisting of a linear gradient from 100% A to 100% B in 10 min and maintaining B for another 15min. Solvent A consisted of 70:20: 10 methanol : water: water + ion pairing agent (v/ v), the latter solvent in a concentration of 1.5 g of tetrabutylammonium acetate and 0.96 g of ammonium acetate in 100 ml of water (Mantoura & Llewellyn 1983). Solvent B consisted of 60:40 methanol :ethyl acetate (v/v). Eluting pigments were quantified by fluorescence in a Hitachi F- 3000 Fluorescence Spectrophotometer fitted with a flow-through cell, with excitation beam at 410 nm and emission at 680 nm. Pigments were identified by their fluorescence excitation spectra (Table 2 ) . The HPLC column was calibrated with pure pigments prepared as in Vernet & Lorenzen (1987) from a culture of Thalassiosira nor- denskioeldii, with extinction coefficients as in Lorenzen & Downs (1986) for chlorophyll degra- dation products, Jeffrey & Humphrey (1975) for chlorophylls a and c ~ + ~ . Because of a lack of a specific absorption coefficient, chlorophyll c3 was 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 s h w n in Fig 2 Spectra o f the pigments were measured in the eluent in a Row-through cell attached to the 5pectrofluorometcr. Peak Pigmcnc Retention FI uorescence number time ( m i n ) maxima ( n m ) I 3 4 > h 7 X I 0 11 C'hloroph\ll r dcribalivc Chlorophyllide o Chloroph>ll c Phaeophorbidc a-like (a:) Phaeophorbidc d - l i k e ( a , ) Phaeophorbidr a-like ( a , - < ) Chlorophyll Q + c derivatives Chlorophyll u derivative Chlorophyll u Phaeophytin a-like ( a , ) Phaeophytin a-like ( a l ) h Y X 0 X Y 9 5 10.4 12.1 14.0 14.6 15.0 l Y . 5 11.0 chlorophylls c , even though a large error might be expected using this approach (Jeffrey & Wright 1987). Photooxidation estimates of phaeopigments were obtained using material collected in the 100- m traps in June 1987. Samples from the traps were diluted with filtered seawater. shaken t o homogenize. and incubated in 250ml Pyrex bottles. Eight bottles were exposed t o sunlight in an incubator placed o n deck. Temperature was kept at 0 % 1°C with running seawater from the ship's water intake. O n e bottle was wrapped in aluminum foil and kept in the refrigerator. in the dark. at 2"C, as control. The pigment content was measured at 3. 6 . 12. 24. 36. and 48 hours of incubation. Photooxidation constants. k , . were calculated as in Welschmeyer & Lorenzen (1985). Phytoplankton growth and zooplankton graz- ing were estimated from pigment budgets. In the summer cruise of 1988. steady state was assumed and the simplified equations presented in Welsch- meyer & Lorenzen (1985) were used. Chlorophyll sedimentation from the euphotic zone was not assumed to be zero. and was estimated as C , C-', where C , (mg chl a m-' d - I ) is the chlorophyll flux to the sediment traps and C (mg m-') is the integrated chlorophyll in the euphotic zone. In the spring of 1987. during the bloom. equations were solved numerically. including chlorophyll sedimentation from the euphotic zone and accounting for changes in the depth of the euphotic zone as expressed in Laws et al. (1988). Pigment concentration was integrated to the 454. 585 437. 624. bb5 450. 586,634 425. 666 414. 614. 662 4OX. h24. 666 442. 462. 626. 667 435. 624. 666 435. 626. 667 117 5. 667 417 5, 666 depth of 1 % incident radiation, defined as the depth of the euphotic zone. Pigment estimated by the Turner Designs fluorometer was used for this analysis because H P L C data for water column phaeopigments were not available for June 1987. Results H y d r o g r a p h y . Spring c o n d i t i o n s Two stations were visited during the spring of 1987 (Fig. 1). Stns. 947-987 were situated in Atlantic waters during a bloom of Phaeocystis p o u c h e t i i . with chlorophyll a concentrations of 4 to 6 mg m-3 from the surface to a depth of 60 to 80 m. At this station stratification was very weak, nitrate was detectable through the mixed layer, and the euphotic zone (1% isolume P A R ) extended t o 18 m (Wassmann et al. 1991). Stns. 941-994 were located in an area under the influ- ence of the Polar Front (Rey & Loeng 1985) and close to the ice edge. Stn. 941 was similar t o Stn. 947 but with only 1.3 mg chl a m-3 in the t o p 20 m of the water column. T e n days later, at Stn. 994, a strong subsurface chlorophyll a maximum had developed at 4 3 - 4 5 m . at the depth of a strong halocline. d u e t o surface meltwater. Nitrate was depleted in the mixed layer and t h e depth of 1%' isolume ( P A R ) was 41 m . Chlorophyll a con- centrations averaged 0.5 mg m-3 in the mixed layer and peaked at 12 mg m - ' at the maximum. This temporal variability in the chlorophyll profile Phytoplatiktori d y n m i c s in the Barents Sea 133 like pigments were found consistently in the water column and sediment traps (Fig. 3). The nomenclature corresponds t o Vernet & Lorenzen (1987) also used by Downs (1989) and Hurley & Armstrong (1990). Two phaeopigments, not named in Vernet & Lorenzen (1987), less polar than phaeophorbide a 3 , were named a4 and a 5 , as in Downs (1989). Phaeophorbide a5 was not always well resolved from a4, the most abundant of the two pigments ( p e a k 6 in Fig. 3). Phaeo- phytin a l and a2 ( p e a k s 10 and 11 in Fig. 3) were present in all samples. A third minor form eluted after a l , but was not quantified. I present here quantification of t h e more abundant phaeo- phorbide- and phaeophytin-like pigments, a 2 , a 3 and a 4 + 5 and a , and a,, respectively. suggests strong advection in the area (Wassmann et al. 1990), precluding the use of the pigment budget model at this station. Summer conditions The stations visited in July 1988 were located in Atlantic waters (Fig. 1) and had already experi- enced &he spring bloom. Of the two, Stn. 885 had a deeper mixed layer (30 m), and a lower density gradient at the pycnocline (Wassmann et al. 1991). Nitrate concentrations were undetectable throughout the mixed layer and a nutricline was established between 20 and 75 m. Chlorophyll a concentrations were 0 . 9 m g m-3 in the mixed layer and had a subsurface maximum of 1.6mg n r 3 a t the t o p the nutricline, a t a depth of 30 m, with a secondary maximum a t 6 0 m (Fig. 2D). This station presents characteristics of late bloom conditions in the Barents Sea when phyto- plankton distribution changes from high con- centration in the mixed layer to a d e e p chlorophyll maximum at the nutricline (Thingstad & Mar- tinussen 1991 this volume). Station 864, further north, had a shallower mixed layer (20 m) and a stronger density gradient than Stn. 885. Tem- perature profiles revealed a warming of surface waters (5°C) over colder water (2.7"C). Nitrate concentrations were also undetectable at the mixed layer. A nutricline was present from 50 to 100m (Wassmann e t al. 1991). Chlorophyll a concentrations were low in the mixed layer (0.2 mg m-3) and peaked at about 75 m with a concentration of 1.2 mg m - j at the depth of maxi- mum nutrient gradient (Fig. 2D). This station represents summer, or postbloom, conditions in the Barents Sea (Thingstad & Martinussen 1991). The euphotic zone, calculated as the depth of 1% isoline for P A R , extended t o 37 and 2 5 m for Stns. 864 a n d 885, respectively. While the chlorophyll maximum during the late bloom was at the bottom of the euphotic zone (Stn. 885), the chlorophyll maximum in the postbloom (Stn. 864) was well below the 1% isolume for P A R (Fig. 2A and D). Although the exact position of the chlorophyll a maximum might have been lost due to low resolution in the sampling (depths sampled were only 50,75 and 100 m), it was situated below the 0.1% isolume for P A R (55 m). Phaeopigment diversity Five phaeophorbide-like and three phaeophytin- Pigments in seston The vertical profile of accessory chlorophylls fol- lowed that of chlorophyll a (Fig. 2 A and D). The abundance of chlorophylls c1 +, and c3 at Station 885 during the late bloom suggests a dominance of diatoms over prymnesiophytes (Jeffrey & Wright 1987). T h e ratio of chlorophyll c3 :chlorophyll c 1 + 2 (w/w) integrated over the t o p 1 0 0 m was 0.1. Stn. 864 was dominated by chlorophyll ci- containing algae, probably prymnesiophytes (Jeffrey & Wright 1987). T h e ratio of chl c3:chl cl+2 (w/w) in the upper 100 m was 0.91. A ratio of approximately 1.0 is commonly found in cul- tures of prymnesiophytes, suggesting that most of the chl c 1 + 2 is mostly c 2 from the prymnesio- phytes. Deeper in the water column, a t the depth of the chlorophyll a maximum, chlorophyll c , + ~ become more abundant, suggesting more diatoms at the nutricline. Vertical distribution of phaeopigments was similar to that of chlorophyll a. Maximum con- centrations coincided with the chlorophyll a maxi- mum at both stations although a t Stn. 885 the deep maximum ( 6 0 m ) was more conspicuous than the shallow o n e (30 m). Phaeophorbide a 4 + 5 was the most abundant phaeopigment in the euphotic zone at both stations, followed by a2 and a,. Below the euphotic zone, the stations differed. At Stn. 885 phaeophorbides a3 and az became more abundant while phaeophorbide a 4 + 5 stayed dominant in the postbloom situation (Stn. 864). Phaeophytins presented a similar distribution t o that of the phaeophorbides (Fig. 2C and F ) but were more abundant during post-bloom con- 134 M. Vernet ditions (Stn. 864). Phaeophytin a , was generally more abundant than phaeophytin a,. Pigment sedimentation The two stations in July of 1988 presented dif- ferent patterns of sedimentation for chlorophylls and phaeopigments (Table 3 ) . Phaeopigment sedimentation (all forms of phaeophorbide and phaeophytin combined) was always higher than chlorophyll a sedimentation for any given depth sampled. During the late bloom (Stn. 885) chloro- phyll a sedimentation was maximum at 40 and 9 0 m and decreased at larger depths. Phae- opigment sedimentation was lower at 4 0 m and was higher at 9 0 m and deeper. A t Stn. 864, during postbloom conditions, sedimentation of all pigments increased 5-fold from 60 to 100 m . T h e 0 25 CI E 5 so 8 - 0 75 100 ~rr.di.nc~ (EIn.1 mead")- 1 . 1 . -- 0.0 0.6 1 .o 1 .s 2.0 Chl-. (rQA - Chl-c (!Ae/l) - l . l . l ' ' . j 0.0 0.6 1 .o 1 .s 2.0 1 . 1 . " 0.0 0.6 1 .o 1 .s 2 .o Chl-CJ (rQ/l) similar pattern of both chlorophyll u and phaeo- pigments suggests that t h e chlorophyll a maxi- mum at about 75 m was the main source of sedi- menting matter a t this station. Sedimentation rates of phaeopigments showed different patterns among pigment forms and sta- tions (Table 3 ) . Phaeophorbide a 3 was the most abundant degradation product in sediment traps. The only exception was a t 60 m at Stn. 864 where phaeophorbide ad+ 5 showed the highest sedi- mentation rate. Phaeophorbide a? had maximum sedimentation rates in the t o p 100 m during late- bloom conditions. with decreased sedimentation rates with depth, while the opposite was observed in postbloom conditions (Stn. 864). Phaeo- phorbide u 3 had maximum rates of sedimentation at 90 or 100 rn. A t greater depths, t h e pattern of sedimentation differed for both stations. remain- 0.00 0.03 0.06 0.09 0.12 0.15 Phbld. 2 I rgA) A-A-4 Phbld. 3 (Llg/l) tf. 1 . 1 . 1 . . . I , J 0.00 0.03 0.06 0.09 0.12 0.16 1 . 1 . 1 . ~ . 1 , 0.00 0.03 0.06 0.09 0.12 0.15 Phb- 4+6 ( pa/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 i n ( A ) and (D). Phytoplankton dynamics in the Barents Sea 135 0 25 I CI E g 50 0 a 75 100 0.00 0.02 0.04 0.06 0.08 0.10 Phytln 1 (up/I) A 4 - A 0.00 0.02 0.04 0.00 0.08 0.10 Phytln 2 ( p g / l l tt. 0 25 - I E 5 50 8 a 7 5 100 0. i f I ' I * ' I I 1 , I \ > 0.09 0.06 0.00 0.12 0.15 Phblda 2 ( p g / l ) C-CI 1 L l , l , , , , , , 0.00 0.03 0.06 0.09 0.12 0.15 Phbld. 9 (pg/I) tt. I . I I l , I . I , l 0.00 0.03 0.06 0.00 0.12 0.15 0 25 1 E 5 50 a a u 0 7 5 tY ST.885 I I 100 I , I , / , , , 6 8 10 0 2 4 Irradlanco (Elf181 m-* d-'I--- 0.0 0.5 1 .o 1.5 2.0 Chl-8 ( pgA) l I I . l , I I 0.0 0.5 1 .o 1.5 2.0 Chi-c ( pg/l) - I I I I 1 , I I 0.0 0.5 1 .o 1.5 2.0 Ch1-d ( pg/l) - 0 2 5 - E 5 5 0 a e 0 u 7 5 100 --- 0.00 0.02 0.04 0.06 0.08 0.10 Phytln 1 (sg/l) 0.00 0.02 0.04 0.06 0.08 0.10 PMd. 4+6 ( pa/l) Phytln 2 ( p g / l l 0-0-0 136 M . Vernet 5 10 15 20 25 TIME (rnin) F i g . 3. Chromatogram zhouing chloroph>ll a and chlorophyll degradation products from 3 5edirnent trap sample collected i n July 1988 in the Barents Sea Pigments were analyscd with a reverse-phase HPLC and detected by Ruorcscence with exci- tation wave length at 42Onrn and emission at 680nm. Peak identities correspond to those in Table ?. ing high at Stn. 885 while decreasing at Stn. 864. Phaeophorbide a.,, increased their sedimen- tation rates with depth. with the exception of 100m at Stn. 864 where rates peaked. Sedi- mentation rates of phaeophytin a ? , the form least abundant in the water column. were always equal to or larger than those of phaeophytin a , . T h e pattern of sedimentation of the 2 phaeophytins was similar t o that of phaeophorbide ~ 2 . In general, maximum rates of sedimentation were found at 90 and 100 rn at Stns. 864 and 885 respect- ively, immediately below the depth of the pigment maxima, where diatoms were more abundant. Phaeopigment photoxidation rates The results from the 3 experiments were com- bined and the resultant first o r d e r photooxidation decay constant, k , (m? mol-I) was computed. Photooxidation rate constants vary among the individual chlorophyll degradation forms by a factor of 2 . from 0.009 to 0.015 m' mol-l (Fig. 4 ) . The average photooxidation rate constant for all pigment combined (SUM P H A E O ) was 0.012 m' mol-'. Pigment model The estimations of phytoplankton growth rate and zooplankton grazing during spring and sum- mer based on the pigment model of Welschmeyer & Lorenzen (1985) a r e shown in Table 4. Phyto- plankton during the bloom of Phaeocystis pou- chrtii i n 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 . 0 5 4 . 0 6 d - ' ) dominated over microzooplankton grazing (0.01-0.02 d - I ) , accounting for approximately 35% of the phyto- plankton 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- phyll accumulated in the euphotic zone. When compared to growth rates estimated from I4C incorporation, assuming a C : chla ratio of 75 from the P O C data ( F . Rey, unpubl. data) and growth calculations according to Eppley (1972), the model underestimated phytoplankton growth by 3 5 % . D u e to the lack of independent estimates of the phytoplankton C : chla ratio, it is not poss- ible to determine how much pigment might have been lost during grazing (i.e. Lopez et al. 1988). A loss of 33% though is expected during macro- lankton grazing (Downs 1989) and seems t o be a representative pigment loss term in the spring bloom (Laws et al. 1988). Estimates of phytoplankton growth rates for the summer were a n order of magnitude lower than for spring (Table 4). Macrozooplankton grazing rates were also an o r d e r of magnitude lower than in the spring. while microzooplankton grazing rates were about the same. In late bloom conditions (Stn. 885), where diatoms dominated in the water column, micro- and macrozooplank- ton grazing were comparable. T e n percent of the chlorophyll sank out of the euphotic zone and about 8% still accumulated. In postbloom con- ditions, where small flagellates were dominant, microzooplankton grazing accounted for 85% of the phytoplankton growth, while 7 % sank o u t of the euphotic zone, and there was almost no net accumulation of phytoplankton in the euphotic zone. N o radiocarbon incorporation data a r e available from this cruise in o r d e r t o compare growth estimates. Discussion Arctic phytoplankton Phytoplankton growth at the ice edge of polar regions is characterized by a n 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 i n 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 Phbide 3 Phbide 4 + 5 Chi a Phytin 1 Phytin 2 Sum Phaeo Phbide 2 Phbide 3 Phbide 4 + 5 Chl a Phytin 1 Phytin 2 60 0.45 0.42 0.90 13.67 0.86 3.11 I00 I .29 2.85 4 09 54.83 2.83 2.22 0.48 0.1 0.3 1.2 2.5 0.2 0.2 2.0 24.3 7.0 15.9 2.5 4.5 2.0 0.22 0.71 1.33 0.18 0.42 0.64 I .55 8.53 1.71 0.29 0.88 2.03 0.23 Sum Phaeo 13.28 40.3 303.0 Phbide 2 230 1.29 1 .x 1.40 Phbide 3 Phbide 4 + 5 Chl a Phytin 1 Phvtin 2 2.85 5.8 4.09 4.0 54.83 2.5 2.83 1 . 1 2.22 I .4 2.04 0.98 0.05 0.39 0.63 885 Sum Phaeo 13.28 21.7 163.0 Phbide 2 40 0.94 1.7 181 Phhide 3 0.71 5.5 7.75 Phbide 4 + 5 I 3 9 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 Phbide 4 + 5 Chl a Phytin I Phvtin 2 3.20 47.95 I .95 1.66 3.08 Sum Phaco 12.95, Phbide 2 250 3.01 Phbide 3 Phbide 4 + 5 Chl a Phytin 1 Phytin 2 Sum Phaeo 3.20 3.08 47.95 1.95 I .66 12.99 17.6 7.8 2.3 0.8 1.4 28.6 0.7 15.3 7.2 2.5 0.9 1.1 25.2 5.50 2.53 0.05 0.41 0.84 220.0 0.23 4.78 2.34 0.05 0.46 0.66 194.0 138 M . Verne1 A .. Phbide 4 O.00t . a e . I a = 0083 J -3 00 0 40 80 120 160 (rn2Einst . 1 ) Phytin 2 o.00T = I hm E l R 2 = 0 4 9 a = 4 3 1 - -1.00 -3.00 0 40 80 120 160 (m2Einst -l ) Phbide 3 O . O O t 0 3 R z = 0 8 5 a = 4 3 1 a -3 00 0 40 80 120 1 i0 (rn2Eins.t -l ) Phytin 1 O . O O t * . 1 J k = 4 0 1 R’= 069 -3 00 0 40 80 120 160 (rn2Einst-’ ) SUM PHAEO 0.00 0 a = a.z? -. .,- 0 40 80 120 I s 0 (m‘Einst -‘) period during the spring d u e to increased sta- bilization of the water column. sun angle and daylength ( D u n b a r 1981; Rey e t al. 1987; Nie- bauer & Alexander 1989; Sakshaug 1989). In the Arctic, and in particular in the northern part of the Barents Sea, the bloom crashes after nitrate has been stripped from the mixed layer and marks the onset of the summer period which is charac- terized by a subsurface chlorophyll a maximum near the nutricline. T h e stratification of water is Fig. 4. Estimation of photooxidation rate constants for the chlorophyll degradation products abundant in the water column and sediment trap matter. Data include three experiments incubated on deck in June 1987 from material collected in 100-m traps at Stns. 941-994 and 947-987. Temperature was maintained at 0 ? 1°C with running seawater from the ship’s intake. Peak 4 is a mixture of phaeophorbide (I,+%. SUM PHAEO ( F ) is the average photooxidation rate constant for all the phaeopigments combined. either d u e t o ice melting at t h e ice edge or t o warming of surface layers, as in t h e case of Atlan- tic waters in the southwestern a r e a of the Barents Sea (Skjoldal e t al. 1987; Loeng 1989). Winter and summer are generally dominated by small flagellates while spring blooms a r e d u e t o either diatoms and/or Phaeocystis poucherii (Rey e t al. 1987). While diatoms a r e generally present in the Atlantic waters of the Barents S e a , P . pouchetii is dominant in ice edge blooms (Wassmann e t 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, 3 s 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% 0 1 8 1990), either after a diatom bloom, when silicate becomes limiting for diatoms, or from the onset of the bloom. Similar observations have been made in the Greenland Sea (Cota et al. 1990) and in the waters around Iceland (Stefansson & Olafsson 1990). Diatoms were dominant in the blooms of Atlan- tic waters in June of 1987 (Vernet unpubl. data) and during late-bloom conditions in July of 1988 (Stn. 885). Single cell prymnesiophytes (i.e. Emi- liana huxleyi) were present in pre-bloom con- ditions in May 1987 (Vernet unpubl. data) and increasingly dominant from late-bloom to post- bloom in July 1988 (Stn. 864). At the ice edge in May-June 1987, more than 95% of the plankton consisted of P . pouchetii cells (C. Hewes, pers. comm.). The distribution of accessory pigments gave a good approximation to characterizing these phytoplankton assemblages in the Barents Sea (Fig. 2 ) . Plankton dominated by diatoms were rich in chl c , + ~ (Stauber & Jeffrey 1988), while those with prymnesiophytes such as E . huxleyi and P . pouchetii had chl c3 in addition to chl c2 (Jeffrey & Wright 1987). With respect to car- otenoids, E . huxleyi has 19' hexanoyloxyfu- coxanthin as the main carotenoid (Vernet 1989). Diatoms and P . pouchetii have focuxanthin (Wassmann et al. 1990). The difference in dom- inant carotenoid within the prymnesiophytes makes it possible to differentiate them. Large cells such as diatoms and the colonial form of P . pouchetii dominate the spring bloom, at which time there are shallow mixed layers, nitrate is present in measurable concentrations, and the density stratification is weak. On the other hand, small flagellates characterize deep or nutrient-depleted mixed layers, encountered in either pre- or postbloom conditions. In this study, large diatoms were abundant in late spring (Stn. 885) but were displaced by prymnesiophytes in the mixed layer as nitrogen became low. These diatoms still grew at the depth of chlorophyll maximum in summer conditions (Stn. 864), when irradiance was low but rates of nutrient supply were probably high. This scenario supports the hypothesis that large cells can grow in environ- ments where there is an increase in the rate of nutrient supply (Thingstad & Sakshaug 1990). Chlorophyll degradation The more abundant forms of chlorophyll a degra- dation found in seston and sedimenting particles of the Barents Sea (see Fig. 2 ) are similar to the forms found in temperate coastal marine waters (Klein & Sournia 1987; Vernet & Lorenzen 1987; Downs 1989; Roy & Poulet 1990), lakes (Car- penter et al. 1986; Hurley & Armstrong 1990) and sediments (Brown et al. 1977). The uniformity of components suggests common catabolic pathways in aquatic environments (Hendry et al. 1987). In Arctic waters, as in other areas of the ocean, the main pathways of chlorophyll degradation involve biotic and abiotic factors. Oxidizing and non- oxidizing enzymes from either the alga itself or a grazer that has ingested it, light, bacterial activity, and oxygen are the main degradative agents (Hendry et al. 1987). The last two sources can be 140 M . Veriier considered secondary in short periods of time (Downs 1989; Roy & Poulet 1990). particularly in polar waters (Wassmann e t al. 1991). In the euphotic zone, light plays a main role in the degradation of chlorophyll and phaeopigments associated to detritus. Pigments a r e degraded to colorless compounds (Struck et al. 1990). the main product of photooxidation (SooHoo & Kie- fer 1982; Welschmeyer & Lorenzen 1985; Vernet & Lorenzen 1987; Downs 1989). In the absence of light, below the euphotic zone. enzymatic activity resulting from zooplankton grazing may be the main factor of chlorophyll degradation. Activity from cellular enzymes. such as chlorophyllase. dephytylizes chlorophyll a in diatoms (Jeffrey & Hallegraeff 1987). From chlorophyllide further enzymatic activity has been found to produce pyropheophorbide via phaeophorbide in cultures of Chlorella fusca. Pyrophaeophorbide. the end product, was found to be very stable in the dark and thus accumulated (Ziegler e t al. 1988). It is clear that further studies are needed in order to characterize the different forms of phaeophorb- ide-like molecules and other degradative forms (Matile et al. 1989). The constancy of the mol- ecules analyzed, common to so many environ- ments, justify the effort. Photooxidation rates of chlorophyll degr2.- dation seem to follow first-order kinetics (SooHoo & Kiefer 1982; Welschmeyer & Lorenzen 1985). At O'C, photooxidation rates of individual phae- opigments vary by a factor of 2 (Fig. 4A-D). In the Barents Sea. phaeophorbide a 3 had the highest rate of photooxidation, followed by phaeophorbide a! and phaeophorbide a , . T h e 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 a 2 and a 3 , although the constants were, on the average. 3 to 5 times higher. A n important corollary of the difference in photooxidation rates of phaeopigments is that the distribution of phaeopigments in the euphotic zone has to be interpreted in light of these differences. where the abundance is a function of the balance between production and loss rates. Distributions depicted in Fig. 2 and photooxidation rates in Fig. 4 suggest that phaeophorbide a,, can accumulate twice as fast as phaeophorbide a 3 for a similar production rate. and may account in part for their abundance in the euphotic zone. Total photooxidation rate can be calculated as the decay rate of the corn- bined pigments (Fig. 4 F ) . For a more accurate calculation of the photooxidation rate of the whole phaeopigment assemblage we should include the relative contribution of each indi- vidual component. Photooxidation rates measured in this study at 0°C are lower than previously published data for temperate waters (SooHoo & Kiefer 1982; Welschmeyer & Lorenzen 1985; Downs 1989) and support the hypothesis of temperature depen- dence. Welschmeyer & Lorenzen (1985) and Downs (1989) found photooxidation rates to be independent of temperature. T h e authors suggest that the source and type of phaeopigment are a probable cause of the variability observed. T h e rates measured in this study suggest otherwise. Individual rates of phaeopigments measured by HPLC and the combined photooxidation constant show lower degradation rates at lower tem- peratures. Fig. 5 shows a n Arrhenius plot includ- ing all the published k, values from marine environments where temperature has been measured. They have been converted t o units of m' mol-' (Table 5). T h e regression obtained is similar t o the o n e by SooHoo & Kiefer (1982). About 35% of the variance is still unexplained suggesting that other variables, such as type of light sensor, type of dominant form of phae- opigment, calibration of the fluorometer, incident a = 4 7 7 r2= 0% ~ 3.3 3.4 , 3.5 3.6 3.7 rn I 0.01 + - 10 -3(aK-1) T FIR. 5 . Arrhenlus plot of the photooxidation rate constant as a function of temperature. Estimates from marine waters have hcen pooled: (solid squarc) SooHoo & Kicfer (19x2): (cross) Wclschrncyer & Lorenzen (1985): (open square) Downs (19x9): (triangle) Vcrnct & Mitchell (19YU): (asterisk) this study. Tem- perature range from -0" to 28°C (see Table 4). Statistics and \driancc cxplaincd arc similar to those ohtaincd by SooHoo & Kicfcr (19x2). Phytoplankton dynaniics i n the Barerits Sea 131 Table 5 . Summary of the first order photooxidation decay constant of phaeopigmcnts Source k , . 10.' Substratc (m'/Einst) ~~~ ~ Temperature ~ ~ SooHoo & Kiefcr (1982) Welschmeyer & Lorcnzcn (1985) Barents Sea (this study) Vernet & Mitchell (1990) Downs (1989) 1.1-8.8 Scston fecal pcllcts 6.75 Scston 1.20 Sediment trap 1.87 Scdiment trap 3.693.9 Scdimcnt trap & 2 8 T -Y-?VC -1-+2"C - 1-+2"C 1+21"C spectral irradiance, and probably size of the par- ticles containing phaeopigments, can introduce uncertainty in this type of measurement. The lack of a significant temperature dependence in photooxidation rates in Welschmeyer and Lorenzen (1985) and Downs (1989) studies may be due t o the narrower range of temperatures studied and the logarithmic relationship between these 2 variables. Accurate values of photooxidation rate con- stants become increasingly important at lower temperatures. A sensitivity analysis showed that the total contribution of microzooplankton graz- ing to total grazing in the pigment model decreases rapidly at lower values of k, (Fig. 6). The model is then most sensitive for low photo- oxidation rate constants, in the range of values measured for Arctic waters. Specific forms of chlorophyll degradation seem to be quantitatively related to the type of phyto- 0.21 8.100 ' 0.02 ' 0.04 ' 0.06 ' 0.08 ' 0.iO k , (m2 Einst-') Fig. 6. Temperature dependence of photooxidation ratc con- stant in the pigment budget model (Welschmcyeer & Lorenzen 1985): scnsitivity analysis of the contribution of micro- zooplankton grazing (g) to total grazing (g + g') as a functlon of the photooxidation rate constant ( k , ) , Arrows indicatc three photooxidation ratc constants: this study (0.012 m2Einst-'). SooHoo & Kiefer (1982) (0.037 m'Einst-') and Wclschmeycr & Lorenzen (0.0675 m?Einst-'). plankton present. Phaeophorbide was more abundant in the station dominated by prym- nesiophytes while phaeophorbide a3 was pro- duced by degradation of diatoms. It is not possible to differentiate with the present sampling design if the degradation is originated by enzymes in the phytoplankton or in the grazers if we assume a close coupling between phytoplankton groups and types of grazers. T h e dominant form of phaeo- phorbide related to the pair alga-grazer is present not only in the seston but also in the large particles that sink out of the surface and are caught by the sediment traps. If, as hypothesized by Shuman (1978) and Welschmeyer & Lorenzen (1985), phaeopigments in t h e seston a r e mainly d u e t o microzooplankton grazing while sinking faecal pellets originate mainly from macrozooplankton, the dominance of the same phaeopigment both in the water column and sediment t r a p sug- gest that the pathway of chlorophyll degradation is related more to the alga than t o the grazer. Sedimentation of the most abundant phae- ophorbide a in lakes was d u e t o 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- todetritus, or through zooplankton fecal pellets. Intact phytoplankton cells contain almost exclus- ively non-degraded chlorophyll a pigments while the pigments of faecal pellets a r e mostly phaeo- pigments (but see Wassmann et al. 1990). Never- theless some undegraded chlorophyll a in the sediment traps could originate from faecal pellets (Vernet & Lorenzen 1987). In this way, estimates of cell sinking based o n chlorophyll a sedi- mentation rates would b e maximum. Maximum sedimentation rates of phaeopig- 142 M . Vernet ment measured below the chlorophyll maximum at both stations suggest that most of the defecation of pigments occurred while zooplankton were feeding at the chlorophyll maximum, as shown by Welschmeyer et al. (1984) and Dagg et al. (1989) i n coastal areas. If the active transport of pigments by zooplankton to depth through vertical migration is minimum (Dagg et al. 1989), sedi- mentation rates at depth are dependent mostly of the remineralization or reingestion of pigments by other plankton at mid-depth. The higher changes observed from 100 to 230 m at Stn. 864 suggest higher recycling of sinking organic matter in the summer with respect to late spring (from 90 m to 250m at Stn. 885). The constant sedimentation rate of pigments below 150m at both stations (except phaeophorbide a 3 ) indicate that most of the transformation may occur immediately below the maximum pigment flux. Although all forms of phaeopigment were found at all stations, there seems to be a quan- titative relationship between some phaeo- phorbides and the type of phytoplankton. Phaeo- phorbide a3, with high and constant sedi- mentation rates below 100111, seems to be associated to large particles that sink fast and are not recycled at mid depths. These results agree with higher presence of this pigment in seston associated with larger cells, i.e. diatoms, at the chlorophyll a maxima at both stations. Phae- ophorbide a,,+ is proportionally more abundant where prymnesiophytes dominate, at Stn. 864, but it is also related to fast sinking particles, particularly at Stn. 885. In general, mid-water recycling seems to be more important at Stn. 864. during summer conditions, although a lack of sampling at intermediate depths makes these con- clusions tentative. Phytoplankton population dynamics The rate of phytoplankton growth estimated by the pigment budget model during the spring (Stns. 947 and 987) is about 65% of the estimate using radiocarbon incorporation. These numbers are within what is expected if we assume a pigment conversion efficiency of about 65% from a large phytoplankton to a large grazer (Shuman & Lor- enzen 1975; Welschmeyer & Lorenzen 1985; Laws et al. 1988; Downs 1989). These numbers seem to indicate that chlorophyll budgets are good indicators of phytoplankton dynamics dur- ing spring bloom. On the other hand, phyto- plankton growth rate estimates for summer sta- tions at the Barents Sea (Stns. 864 and 885) are lower than might be expected for phytoplankton growing at high irradiance in stratified waters. Growth rates estimated from primary production measured in the same area in June-July 1979 (Ellertsen et al. 1982). and assuming a C:chla ratio of 100. are in the order of 0 . 0 6 4 . 1 d-l, 2 to 10 times higher than the estimated rates (Table 4). Similar discrepancies are observed in tropical environments. Laws et al. (1988) suggest that phytoplankton growth rates in the Central Pacific might be underestimated by 6670 if we compare data from the pigment model (Welschmeyer & Lorenzen 1985) to the direct measurements of growth rate (Laws et al. 1987). Both tropical and Arctic data indicate that where nutrient recycling is important and where small algae and small grazers are dominant, there is a higher loss factor in the conversion of chlorophyll t o phaeopig- ments. An alternative scenario could be that the observed phaeopigment :chlorophyll ratio would be averaged over a longer food web each of them with a 35% loss in each step of the food web. Independent of the reason, summer situations in the Arctic seem more similar to tropical stations with an average conversion factor larger than 66%. These results are thus in agreement with studies where pigments were useful tracers of macrozooplankton grazing (Dagg et al. 1987) while the opposite is true for microzooplankton (Klein et al. 1986; Strom 1988). During the spring bloom, phytoplankton grew at maximum growth rates for the ambient light and temperature present at that time of year. Growth rate estimates of 0.14-0.17 d-l in 1987 were calculated based on a mean irradiance in the euphotic zone of 1.6611101 m-' d-'. Planktonic diatoms isolated from the Barents Sea, grown at 18 pmol m-2 SKI of continuous light (total daily mean irradiance of 1.55mol m-* d-l), had an average growth rate of 0.17 d-' (Gilstad & Sak- shaug 1990), in good agreement with the model estimates. In conclusion, estimates of phytoplankton dynamics based on chlorophyll budgets can be used with reliability during ice edge blooms of Arctic waters. During summer conditions the model seems to underestimate phytoplankton growth. Mass balances of C are within expected values during both seasons, although the mag- nitude of any given pool must be underestimated during the summer. The model parameters used Phytoplankton dynamics in the Barents Sea 143 for temperate and tropical waters cannot be directly applied to polar areas, in particular the photooxidation rate constant for phaeopigments. A close look at the individual phaeopigments in the water column and sedimenting matter can give insight into phytoplankton-grazer inter- actions. Furthermore, information on phyto- plankton composition based on distribution and abundance of accessory pigments can relate graz- ing to food availability. Acknowledgements. - I thank P. Wassmann for the sediment trap samples, F. 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