Vol. 66: 183-195, 1090 MARINE ECOLOGY PROGRESS SERIESMar. Etrol. Prog. Ser.

Published Seplember 6

Mass sedimentation of Phaeocystis pouchetii in theBarents Sea

Paul Wassmann1, Maria Vernet2, B. Greg Mitchell2, Francisco Rey3

1 Norwegian College ol Fishery Sdence. UnlvenlN of Tromso, PO Box 3083. Guleng, N-9001 Tromse, Norway3 Marine Research Division, A-Oie! Scr1pp> Institution <M Oceanography, University ol California, San Diego, La Jolla,

California &2093, USA9 Institute for Marine Research.. PO Box 1870, N-5024 Bergen, Norway

ABSTRACT: Mass sedimentation of gelatinous rolonies of the prymensiophyte Phaeocystis pouchetiiwere observed In the upper !00 m of Atlantic v> ater in the central Barents Sea. Sedimentation rates ofpaniculate organic carbon and nitrogen as weCl as pigments were the highest recorded so far fromoceanic environments of the North Atlantic or coastal areas of Norway. High relative concentrations ofphytoplankton pigments found in the traps are interpreted as a combination of sinking of Intactphytoplankton cells and undegraded pigments present in macrozooplankton faecal pellets. Evidencepresented in this study implies that the zooplankton community of the Barents Sea was not able tocontrol this phytoplankton spring bloom. The suspended and sedimenting organic matter was rich incarbon and pigments, but poor in nitrogen. Tils U explained by the presence of large amounts ofcarbon-rich mucilage which P. pouchetii colonies develop during their development. In addition todiatoms, sedimentation of a gelatinous phytoplankton species like P. pouchetii may contribute signifi-cantly to the formation of Esrine snow and vertical flux from the euphotic lone. However, degradationof P. pouchetii derived derirus at depths less than 100 m greatly diminishes the likely significance of P.pouchetii blooms in processes such as the carbon flux to the deep ocean and sequestering of COj.

INTRODUCTION

Mass occurrences of the colony-forming, planktonic.prymensiophyte algae Phaeocystis pouchetii havebeen reported since the last century (Lagerheim 1896.Gran 1902). P. pouchetii is described as a eurythermal.stenohaline species, with bipolar distribution. Thespecies develops regular blooms in polar, subpolar andboreal waters (KashMn 1963, Lancelot et al. 1967).There is usually one bloom episode per year and P,pouchetii may, according to Bigelow (1926), be the onlyorganism that rivals diatoms in abundance during thevernal bloom. In the North Sea Phaeocystis bloomsusually appear after diatom blooms and may reachchlorophyll a concentrations of > 20 mg m"3, with dailyproduction ranging from 1 to 4.8 g C m*3 fC*de< &Hegemann 1986, Gieskes & Kraay 1977, B&tje &Michaelis 1986, Veldhuis et aL 1986). Up to 60 % oftotal fixed carbon has been found to be due to P.pouchetii during blooms (Guillard & HeUebust 1971,Lancelot 1983, Eberlein et aL 1985). During blooms thenumerical abundance in Norwegian coastal waters canvary between 40 and 83 % of the standing crop (Salt.

shaug 1972, Haug et al. 1973, Eilertsen et al. 1981,Hegseth 1982).

. Phaeocystis pouchetii is also prominent in the margi-nal ice-edge zone and the open waters of the BarentsSea, where blooms of P. pouchetii, as a general rule,follow a diatom bloom in late spring (Rey & Loeng1985). However, at individual stations and during someyears P. pouchetii may dominate the entire springbloom in the Barents Sea (F. Rey unpubl.) and the.Greenland Sea (L. Codispoti per*, comm.) P. pouchetiihas been characterised as a causative agent respon-sible for the reduction of diatom populations (Smayda1973, Barnard et al. 1984). The impact of a singlespecies like P. pouchetii on the marine food web ofareas like the North Sea and the Barents Sea is obvi-ously considerable (Joiris et al. 1982, Rey & Loeng1985, Lancelot et al. 1987).

Disappearance of Phaeocystis pouchetii, as for anyother blooms in boreal and arctic waters, could becaused by grazing, autolysis, microbial degradation orsedimentation. An antagonistic nature of P. pouchetii toother trophic levels has been suggested (Savage 1932.ZenWevitch 1963, Martens 1981, Schnack et al. 1984).

Inter-Research/Printed to F. R. Germany 0171-8630/90/0066/0183/S 03.00

164 Mar. Ecol. P«:>g. Ser. 66: 183-195, 1990

P. pouchetii has, however, recently been characteredas food for copepods (Weisse 1983, Sargent et al. I&85.Tande & B&mstedt 1987) and was actually preferredwhen offered simultaneously with diatoms (Huntler etal. 1987). These contradictory lines of evidence implythat grazing is likely to contribute to, but no* cause, ihedisappearance of P. pouchetii blooms.

Autolysis and bacterial degradation have been sug-gested as important mechanisms for the disappearanceof senescent P. pouchetii (Guillaid & Hellbust 19-71,Lancelot 1984, Lancelot et aJ. 1987). A significant fric-tion of the carbohydrate-rich, gelatinous material! ofolder colonies of P. pouchetii is regarded as a richsubstrate for bacteria (Veldhuis & Admiraal 1&85,Davidson & Merchant 1987).

The life cycle of Phaeoc}-$ti$ pouchetii (flagella^dand colonial stages), the large amounts of accumula^c-dDOC, and heavy bacterial colonisation of suspendedand sedimenting detntus of P. pouchetii suggests thatP. ppzjcAeti; Die-mass is easily recycled in the upper partof the water column (F. Thingstad pers. comm.). Previ-ous investigations have demonstrated positive buoy-ancy of P. pouchetii (Skreslett 1988), implying thatsedimentation may be unimportant for this specks.Data p:esented here, however, indicate that sedimen-tation of massive blooms of P. pouchetii may dominateits disappearance in late spring in the Barents Sea.

MATERIAL AND METHODS

Data were collected in May/June 1987 during PROMARE Cruise 12 on board RV G. O. Sars' at 2 loca-tions: Station 1(75C 00'N,28 e 37'E; Cruise stns 937, S47and 987; z = 320m) and Station U (74° 29'N, 31° 31' E;

Cruise stns894, 941 and 994; z = 230 m) in the centralBarents Sea (Fig. 1). Station I was in an area dominaiedby Atlantic water, while Station D was in the vicinity ofthe Polar Front, which separates Atlantic from Polarwater. Each location was visited 3 times at II and 17 dintervals for.Stations I and n, respectively. Hydro-graphic profiles were obtained with a Nefl Brown MkIII CTD-profiler mounted with a General OceanicRosette Sampler equipped with 51 Niskin bottles.Sampling depths were selected, on the basis of salinity,temperature and in vivo fluorescence (Sea Tech) at theend of the downward cast

Samples for nutrient analysis (nitrate/nitrite, phos-phate, silicate, ammonia) and suspended biomass (p«r-ticulate organic carbon and nitrogen (POC PON) andpigments) were collected at 15 to 24 depths. Samplesfor nutrients were analysed on board with an auto-analyser, using standard methods (Feyn et aL 1981).Duplicate samples for the analysis of suspended POCand PON were filtered onto Whatman GF/F filten and

20°77'

35

- HO;EN/ // \ >•',/ ' '/ •-•-

/ t

s

70<

20° 35'

Fig. 1. Stations 1 and n in the central Barents Sea. Sobdarrows; Atlantic water; dashed arrows: Arctic water. Dottedline: Polar Front between AlMntic and Arctic Water. Doned

arrows: coastal water close to the Norwegian coast

analysed with an elemental analyser (Carlo Erba,model 1106). Duplicate samples for the determinationof chlorophyll a and phaeopigments were filtered ontoMilh'pore membrane filters (0.45 um) and analysed onboard according to Holrn-Hansen et al. (1965) using aTurner Designs fluorometer (model 10-005) calibratedwith chlorophyll a (Sigma). Seawater containing largeamounts of PAaeoeystis pouchetii colonies is difficult tofilter due to dogging of the filter by mucilage. Presum-ably most of this mucilage was not retained by thefilters (Lancelot & Mathol 1985). Care was taken thatthe negative pressure during filtration did not increaseto more than 0.4 kg cur2. Filtration of each sampleusually took less than 20 min. Water samples werestored cool and in the dark, and filtration was com-pleted less than 6 h after sampling.

Samples for HPLC analysis of suspended pigmentswere collected with 5 or 301 Niskin bottles and filteredonto Whatman GF/F filters. Filtration time of eachHPLC samples was less than 1 h. After filtration, sam-ples were stored at -80 °C until analysis in the labora-tory. Samples were transported on dry ice to San Diego,California. For both analysis, pigments were extractedwith 90 % acetone for 24 h at 4 °C.

A reverse-phase step-wise gradient elution systemWM used for quantitative HPLC analysis ofchlorophylls and photosynthetic accessory pigments

ia et at: Mass seciimentation of Phaeocystis pouchetii . 185

(Vernet & Lorenzen 19B7). Th.-ee solvents wer*employed: 90:10 methanol: wcter (v/v), ^ 94:t>methanol: water (v/v) and 100 % methanol at:trie rat*of 1 ml rain"1. All chemicals were HPLC grade. The firs-isolvent reagent contained a buffer (ammonium acetate-iand the ion-pairing reagent tetra-butyl ammoniumacetate (Mantoura & Llewellyn 1983). The column wa*a 4.3 mm x 25 cm C-18 Econosphere from Alltech with5 nm particles. Pigments were detected by absorbancv:at 440 nm. Pigment concentration was calculated bymanually measuring the corresponding peak are<a(height x width at 14 height).

Pigments in the water column were identified by cc-chromatography with known pigments and by determi-nation of their absorption spectra in the eluent (Wrighi6 Shearer 1984). A second HPLC system was used toqualitatively characterise the pigments in thechromatogram. The" column was a C-18 SpherisortiODS-5, 4.6 mm x 25 cm, with 5 pm particles. Two sol-vents, A and B, were pumped through a column withprecolumn at 1.0 ml min""1 in a linear gradient startingat 100 % A and reaching 100 % B after 12 min. SolventA consisted of 80 : 20 methanol: water (v/v) with 10 %,of the water added containing the ion-pairing reagem(Mantoura & Llewellyn 1984). Solvent B was 60:40methanol: ethyl acetate (v/v). Absorption spectra of theeluting pigments were performed in an Hitachi U-2000spectrophotometer, with a flow-through cell. Phaeopig-ments were estimated in this system.

Macrozooplankton was sampled by vertical net tows(70 to 0 m), sorted under a microscope, and incubatedat 0 CC in the dark in defecation chambers filled withfiltered seawater. After 24 h faecal pellets were col*lected with a pipette and concentrated for pigmemanalysis.

Sedimentation was measured below the euphoticzone at 50 and 100 m depth for periods ranging from 4to 11 d (average 7 d) using double cylindrical PVCtraps with a height of 1.6 m and a diameter of 0.16 m(H/D ratio of 10). No poisons were used during thedeployments. Therefore, some decomposition andgrazing of organic matter inside the traps may havetaken place. The contents of each trap were transferredalong with about 21 of seawater to a bottle andthoroughly mixed before subsampling. Triplicate sub-samples (5 to 100 ml) were taken and filtered for analy-sis of POC, PON, chlorophyll a, and phaeopigmenti.The material from the traps was microscopicallyexamined on board.

The photosynthesis-iTTadiance (P vs I) response ofphytoplankton in the sediment traps at 100m depthwas determined in an incubator which was kept at therelevant in situ temperature. The fight source was a400 W halogen-metal lamp (Osram HQI-T 400 W/DH).Ten different scalar irradiances ranging from 0 to about'

1700 jimol ra~2 s*1 were obtained using neutral filtersmade of plexiglass. An aliquot of 150 ml .of the trapsuspension was'-- thoroughly mixed with 740 kBq(20 MCi) of sodium bicarbonate in automatic pipettesystem. Ten ml of this mixture was added to 11 sepa-rate scintillation vials. Ten vials were incubated for 1 hin the incubator, and 1 vial was wrapped in aluminiumfoil and placed in the cooling water as control.

After incubation, the samples were immediately fil-tered in dim light through Millipore membrane filters(0.45 nm) which were rinsed with filtered seawater.The filters were exposed to fumes of concentrated HC1for 2 to 3 h in a sealed container, after which 7 ml ofOptifluor scintillation cocktail was added. Radioactivitywas measured on board in a Packard Tri-Carb 4430scintillation counter using the channel ratio method forestimating quenching. Photosynthetic rate was deter-mined after subtraction of the dark fixation. Parametersof the P-I curves were determined according to themodel of Platt & Gallegos (1980), using an iterationprogramme.

RESULTS

Hydrographic conditions*

In May/June little stratification had developed etStation I (Fig. 2A). Nitrate in the euphotic zone was <1 jiM at the beginning and was non-detectable at theend of the investigation. This indicates that the summersituation, which is characterised by nutrient limitation,had begun (Fig. 2B). Phosphate also decreased, butwas presumably non-limiting (Fig. 2D). Maximumammonia concentrations up to 2 jiM were observedbelow the euphotic zone (Fig. 2C) and indicate eitherhigher uptake of regenerated nitrogen in the photiczone or higher grazing and regeneration rates of nitro-gen below the photic zone. Silicate was, however,much less depleted than nitrate at the beginning of thesampling period (Fig. 2E), suggesting that diatomswere not predominant during the vernal bloom at Sta-tion I. Active uptake of silicate, most probably bydiatoms, was observed as the silicate concentrationdecreased by half within 1 wit.

Station II was influenced by fresh water from meltingsea ice. This is indicated by the increasing stratificationwith time (Fig. 2F). Nitrate in the euphotic zone waslow (Fig. 2G) as were phosphate and silicate (Fig. 21, J).The ammonia distribution was similar to that of thatStation I (Fig. 2H). The observed silicate depletion indi-'cates that diatoms contributed to an early vernal bloom,

Advection of nutrient-rich (but low-ammonium)water was observed at both stations. This was observedfrom 25 to 75 m depth at Station n in late May, and lesssignificantly from 50 to 100 m at Station I in early June.

186 Mar. EcoL ?Tug. Ser. 66: 183-195, 1990

a, N03(pM) NHJpM) P04 IvW) Si (OH),

278 260 28.2 0 3 6 9 12 3 0.5 10 1.5 20 0 0.2 04 0.6 0.8 0 2 4 6 8

100

150

200

250

300

»*

i

937

- 26 * 7.6 "I&47 987 J

N03 [y P04 Si (OH),

27.8 2BO 28.2 0 3 6 9 12 0 0.5 1.0 1.5 20 0 0.2 0.4 0.6 0.8 0 2 4 6 8

50

100

160

200

o 21.5 • 28.5 * 8.6 "I894 941 994 J*

Fig. 2. Vertical distribution of density (oj, nitrate, ammonia, phosphate and silicate during May/June at Station* I and n in theBarents Sea

Suspended blomass

Pheeocystis pouchetii was a prominent speciei atboth stations and was predominant at Station I. At thetime of the first deployment, an average of 13 500 P.povchetii colonies r1 were found in the upper 50 m{average of 628 cells per colony; C. Hewes pers.

comm.}. Diatoms were also present at both stations,although in low concentrations.

High biomass and pigments from the surface to 70 mat Station I indicate that the vernal bloom was still inprogress (Fig. 3A, C, D). The PON/POC ratio clearlydecreased over time, which might suggest nitrogenlimitation (Fig. 3B). Observed depletion of nitrate in

r.p et al.:-Mass seciunentation of Phaeocystis pouchetii 187

)0 200 400

' POs ?OC (•/!) Ehi « (pg I"1 { ." - Fluorescence- Chi • /Phaeo (w/w)0 0 . 1 0 . 2 0 . 3 0 2 ' - 4 6 . 8 0 1 2 3 4 0 1 2 3 4

50

100

160

200

250

300 -

^?

SJ ?R * * -D • -

o 27937

.5 ' 2.6 * 7.6-^1 j

. , 047 987. J *

0 200 400

POS'POC (t/a). Cm i(pg i"1) . Fkjorticenct ^ CW a/Phuo (w/w)0 C . I 0 . 2 0 . 3 0 3 . 4 6 8 0 1 2 3 4 0 1 2 3 4

50

100

160

200

8.6094

Fig, 3. Vertical distribution of particuloit organic carbon (POC), chlorophyll a (chl a), in vtvo fluorescence, and the relationshipbetween paniculate organic nitrogen and POC (PON/POQ and phaeoplgrnents (chl a/phaeo) during May/June at Station* I and D

in the Barents See ' •

surface waters at Station I (Hg. 2B) supports thishypothesis. Colonial stages of Phaeocystis pouchetiiare however characterised by large amounts of muci-lage rich in carbon and poor in nitrogen (Lancelot et a).1987). The PON/POC ratio may therefore primarilyreflect the dynamics of mucus.production by the P.poucbetii colonies (nitrate was still measurable).

The time development of suspended biomass and

pigments at Station II reflects the progress of a plank-ton community from the end of the vernal bloom to asummer situation in which nutrient limitation was sig-nificant in surface waters. This seasonal transition wascharacterised by a change from uniformly high.biomassin surface waters during the vernal bloom to low bio-.roass in surface waters with a strong subsurface bio-mass maximum in the nutridine (Fig. 3F to I).

388 Mar. Ecol. P?t.g. Ser. 66: 183-195. 1990

The spring-summer transition observed at Station IIwas not observed at Station L Overall, biomass atStation I was relatively high and constant, althoughnutrients did decline. A small but significant decreaseover time in chJ a/phaeo ratios at both stations suggestsan increasing importance of grazing (Table 1). Tb*e> chla/phaeo ratio and total biomtss decreased mere atStation II indicating that grazing may play a role i.^ thedecrease of surface biomass in the spring-summertransition.

The pigment composition, in particular the presenceof chlorophyll c3, reflects the predominance of F-rym-nesiophytes {Table 2). Similar to other prym^-fsio-phytes, Pkaeocystis pcuchetii is characterised bychlorophyll c3 in addition to chlorophyll C) (Jefht-y &Wright 1987). Other accessory pigments observedinclude diadinoxanthins arid low p-carotene. The maincarotenoid found at the ice-edge in the Barents Sex* wasfucoxanthin. This indicates that the Arctic str.v.n issimilar to the P. pouchetn found in the North Sesa (U*.W. Gieskes pers. comm.|, but different from Antarcticstrains where 19'-hexanoyl/ucoiajithin replaces luco-xanthjn as the major light-harvesting pigment (\Vright& Jeffrey 1987).

Piofiles of chlorophyll c (c3-^Ci), fucoxanthin anddiadinoxanthin, the more abundant accessory pig-

ments found at the ice-edge, follow the distribution ofPOC and chlorophyll a at both stations (Fig. 4).

Sedimentation oi organic matter

Vertical loss of organic matter from the euphotic zonewas far higher at Station I than at Station II (Tables 2and 3). The POC, PON and pigment sedimentationrates at Station I are the highest rates recorded from theBarents Sea so far (Wassmann 1989). Significantsedimentation of phytoplankton at Station J is alsosuggested by the variable fluorescence below ?0mdepth (Fig. 3D), Sedimentation rates of organic matterand pigments at Station II (Table 3) were comparable tothose recorded previously during early summerperiods. Sedimented matter was dominated by colonialstages of Phaeocystis pouchetii. This was most evidentfor 50 m depth at Station I. AJso present in the trapswere variable amounts of faecal pellets and phyto-detritus. At Station I a light green, slimy and 4 to 6 cmthick mass of P. pouchetii accumulated in the traps at50 m depth. Loss of DOC from P. pouchetii mucilageduring filtration (Lancelot & Mathot 1985) inevitablygave rise to underestimation of sedimentation rates.

Sedimentation rates deceased significantly between

Table 1. Integrated suspended bionass in the upper 50 m of the water column in the Barents St-a during May/June 1987 (rag =. ~*}.Values a/e averages of the deployment and recovery si.iiions. Also shown are various ratios characterising the quality of orgarJcmetier. Chlorophyll (Chi) a and phaeopigment (Phaeoi data are fiom fluorescence analysis, (a/a): atomic ratio; (w/w): weigh: r«tio

Station

Station I937-947947-987

Station II894-941941-994

Time interval

27 May-2 Jun2-7 Jun

21-28 May28 May-8 Jun

POC

1656019665

137908672

PON

20C414%

13401009

Chl a

366283

16894

Phaeo

127126

4642

PON/POC(av'a)

0.1210.076

0.09?0.116

Chl a/phaeo(W/WJ

2.882.25

3.652.24

Chla/POCfw'wf

0.0220.014

0.012O.Olt

Table 2. Daily loss rates of suspended biomass |%) from the upper 50 m at 2 locations during May/June 1987 in the Barents Seadue to sedimentation

Station

Station I937-947947-989

Station 11894-941941-994

• Chlorophyll

POC

3.474.25

0.670.57

a equivalents (chlorophyll

PON Chl a*

3.315.62

0.630.5&

a + phaenpigment;

2.442.87

1.980.&4

Chic

2.221.31

0.37

Fucoianthin

1.755.19

0.20

D 1 a dinoxaatfain

1.874.86

0.58

•zn et al.: Mass sediimentatlon of Phaeocystis pouchetii 189

Chlorophyll a

0

20

40

60

eo

"E" 100

0 2 a 10

u

20

40

60

eo

inn

•-1 i I t i i

k- ^"-v.

1 -•'

Tr

E

Chlorophyll! c

0 0.4 08 \2 16 2.0 0

Fucoxanthin

1.0 2.0

~-4

I

1 &V.r :^;x1 "r

C

0

1

B

Station I (o 937; • 947; o 937)

Diadinoxanthin

0.05 0.1 0.15 0.2

H

Station D (o 941; • 994)

Fig. 4. Vertical distribution of chlorophyll a. chlorophyll c. diadinoxanthin and fucoxanthin during May/June at Stations I and n Inthe Barents Sea as analysed by HPLC

Table 3. Average sedimentation and standard deviation (%) of parti oil ate organic carbon and nitrogen (POC PON), chlorophyll aand phaeopigments derived from double traps at 2 stations in the Barents Sea during May/June 1987 (mg m~3 d~]). Also shownare ratios characterising the quality of settled organic matter: FON/POC. chl a/phaeo and chl a/POC. Pmu (mg C [mg chl a]"1 h"1)

of the settled maner «t 100 m is indicated

Station

Station I937-947

947-987

Station II894-941

941-994

Depth(m)

50100

50100

50100

50100

POC

575 ±15" 223 ±22

835 ±13198 ±12

93 ±1997 ± 9

49 ±1364± 6

PON

66.3 ±1223.4 ± 14

84.1 ±1023.2 ±11

8.4 ± 2710.2 ±17

6.0 ± 207.3 ± 6

Chid

6.91 2 161.651 10

6.80i 41.631 11

0.80 ± 110.57 ± 9

0.20 x 220.51 ± 3

Phaeo

5.11 ±283.20 ±14

4.94 ±102.57 ± 7

3.43 ±103.54 ± 4

0.67 ± 31.76 ± 3

PON/POC(a/a)

0.0990.091

0.087. 0.104

0.0770.105

0.1220.114

Chi a/phaeo(w/w)

1.350.52

1.400.63

0.230.16

0.290.29

Chl a/POC(w/w)

0.0120.007

0.0080.008

0.0090.006

0.0040.008

* mu

0.4

0.5

0.6

0.2

50 and 100 m at Station I suggesting dissolution, break-down and grazing of the settling matter, in contrast toStation n, where vertical fluxes were more uniform,High chl a/POC ratios indicate a high abundance ofphytoplankton in the traps at both stations (Tables 3and 4). The sedimented maner at Station I was domi-nated by chlorophyll a at 50 m and by phaeopigmentiat 100 m depth while at Station n phaeopigments werealways predominant

The daily loss rates for suspended organic matterdearly indicate the differences in plankton dynamicsbetween Station 1 and n (Table 2). From 3 to 6%suspended POC and PON in the upper 50m wassedimented daily at Station I. At Station n, however, onaverage 0.61 % of suspended POC and PON left theeuphotic zone. Daily loss rates for pigments at Station Iwere more variable than loss rates for POC and PON,but of the same order of magnitude and always < 5 %

190 Mar. Ecol. Pw»g. Ser. 66: 183-195. 1990

Table 4. Comparison of biochemical composition of organw matter from the water column (WC; integrated 0 to 50 m), sedimentedmatter (SM) and combined faecal pellets (HP) of macrozccplankton (CaJanus finmarchicus. C. hyperboreus, Metridia Jonga andThyssanoessa inermis) collected by vertical net tows from. 70 to 0 m. Pigment ratios are based on HPLC analysis. POC/PON: a/a;

pignnent ratios: w/w

Ratios

PON7POCChi a/POCChi a/PONChi a/chl Ci_2 .3

Chi a/fucoxanthinChi a/diadinoxanthinChi a/phaeophytinChi a/phaeophorbide

WC

0.0960.0200.2099.52526

42.6

-

Station ISNt

50 m

0.09300020.0161.071.33

13833.4

1.26

100m

0.09700060.052.172.04

16.411.8077

WC

0.1040.0080.079

14.36.45

667

-

Station IISM

50 m

0.0990.0060.0608.625.55

27.43.840.67

100m

0.1090.0020.0204.283.12

15.63.700 4 4

FP

__

7.692.94

30.31.720.66

{Table 2). Again Station II had. on average, about 5times lower loss rates than Station L

The PON/POC ratio was relatively invariant betweensuspended and sedimenting material for all samples(Table 4). The typical value (about 0.1) is ca 30 % Jessthan the Redfield ratio for exponentially growing p.hy-toplanklon (0.16), as might be expected for caibon-nchcolonies of Phaeocystis pouchetii (Verity et el 19<rl8).The chl a/POC ratio was highest for suspended maricrat Station I and is in the range expected for phvio-plankton during spring blooms. Sediment trap materialat Station I had much lower chl a/POC ratios. At StationII, the chl a/POC ratio in the water column was low, anobservation typical of oligotrophic frstems where dt-tri-tal concentrations are relatively high. The compositionof sedimenting material at Station n was similar to thatobserved at Station I.

The main carotenoids present in seston were Alsofound in copepod faecal pellets and sedimented matter.The ratio of chl a/carotenoids was highest in seston andlowest in sediment traps, as expected if chlorophyll awas the pigment that degraded fastest. The highervalues of chl a/carotenoids at Station n suggest differ-ences in the processes that transform phytoplanktonpigments.

Several phaeophorbide- and phaeophytin-likemolecules were observed in abundance in sedimentingmaterial and faecal pellets as observed in temperatewaters (Vemet 4 Lorenzen 1987). Phaeophorbide wasalways more abundant than phaeophytin and was rela-tively more important at Station n than in Station I.Chlorophyll a dearly dominated sedimentation at 50 mat Station I.

P vs I curves from the sedimented matter at 100 mdepth indicate that much of the sedimented matterconsisted of photosynthetically viable phytoplankton.This is reflected in the Pmu values presented in Table 3.Pm« values from the water column at Station I and II

(0 to 90 m, n = 15) ranged from 0.4 to 1.7 mg C [ragchl a)'1 h~] (average = 1.1; F. Rey unpubl.), Valuesfor sediment trap material ranged from 0.2 to 0.6.

DISCUSSION

Massive sedimentation of organic matter followingphytoplankton blooms has*been documented for bothcoastal and oceanic environments, including polarareas (Schnack et al. 1984, Bodungen et a]. 1986).Ungrazed diatoms and diatom-derived detritus oftendominate vertical flux at the end of the vernal blooia(Smetacek 1985). Slimy colonies of a prymensiophytealgae like Phaeocystis pouchetii have, however, notbeen reported to contribute significantly to the verticalflux of phytoplanklon-derived detritus. P. pouchetii candevelop blooms in water mixed as deep as 60 to 100 m,where diatoms generally do not develop blooms (Sak-shaug & HolnvHansen 1984) and appears to be moreefficient et marginally low b'ght than many otherspecies (Eilertsen et al. 1981, Palmisano et al. 1986).The massive bloom observed in the weakly stratifiedAtlantic surface water at Station I {Figs. 2A and 3D),where more than half of the biomass is below theeuphotic zone, and the deposition of viable, shade-adapted cells as deep as 100m (Table 3), shows theability of these algae to live in low-light environments.

Compared to the marginal ice zone close to the Polarfront, where the phytoplankton spring bloom takesplace in late April/early May, the bloom in the Atlanticwater develops more slowly and peaks about 1 mo laterin May/June (Skjoldal & Rey 1989, Wassmann & Slag-stad unpubl.). This variation in the timing of the bloomis caused by differences in water column stabilisationdue mainly to warming by solar radiation in Atlanticwater, but due to rapidly melting sea-ice in the margi-nal ice zone. These differences in the bloom dynamic*

zn et al.: Mass sedimentation of Phaeocystis pouctietii 191

are reflected by Station I dominated by Atlantic watejand Station II in the marginal ice zone close to the PolarFront. During the investigated period at Station I *spring bloom at its maximum was observed asTeOectevdby the pigment concentrations and Duorescencv(Fig. 3C, D). A senescent stage of the spring bloocnwith rapidly declining pigment concentrations wa=sobserved at Station II (Fig. 3H, I). The observed varia-bility at Station II reflects not only the genera]dynamics of a senescent bloom In a stratified body erfwater, but also the advection of increasingly 'mature1

bodies of water from the Polar Front area as suggestedby variation in density and nutrient concentration*(Fig. 2F to J).

Phaeocystis pouchetii blooms and vertical flux oforganic matter

The sedimentation rates of POC, PON and especiallypigments at Station I (Table 3) are among the highestrates recorded from oceanic environments such as theNorwegian Sea (Bathmann et al. 1987), the Norwegiancoastal current (Peinert et al. 1987), and the NorthPacific (Martin et al. 1987), and are even higher thanrates from the Norwegian coastal zone (Wassmann1984). Compared to oceanic environments like theneighbouring Norwegian Sea the Barents Sea func-tions in terms of magnitude and time variation ofsedimentation rates more like a coastal area. Highvalues of chl a/phaeopigments, chl a/POC and chl a-specific rates of photosynthesis for sedimentingmaterial during this study suggest a large fraction ofthe flux is comprised of viable phytoplankton. Micro-scopic analysis confirmed that Phaeocystis pouchetiiwas the dominant phytoplankton species.

The presence of carbon-rich mucus of Phaeocystispouchetii colonies gives rise to PON/POC ratios wellbelow the Redfield ratio of 0.16 (Verity et al. 1988), asseen in the present results (Table 4). However, chl a/POC ratios are nigh (Tables 1 and 4). The suspendedand sedimenting matter of P. pouchetii blooms is thuscharacterised by low nitrogen and high carbon andchlorophyll a concentrations. To fully utilise the richcarbon source of P. poucbetii derived matter, betero*trophic organisms colonising detritus will require analternative nitrogen source. Profiles of POC, chloro-phyll a, in situ fluorescence (Fig. 3) and in situ beamattenuation coefficients (G. Mitchell unpubl.) indicatethat less than 10 % of surface values of these partial-late variables is present at 200 m depth. High sedimen-tation rates in shallow water and the low concentrationof suspended particulates at depth indicate significantremineralisation at depths less than 100 m, as reflectedby ammonia accumulation in the 50 .to 100m depth

interval {Fig. 2C, H) and decreased sedimentation ratesat 100m (Table3). Remineralisation of P. pouchetiiderived detritus by bacteria requires assimilation ofdissolved nitrogen%compounds. Alternatively, grazersmay consume the sedimenting material, and repack-age as faecal pellets what they did not assimilate.Dense but relatively rare faecal peUets wouJd not con-tribute significantly to any of the particulate variableswe measured at 200 m.

The sedimentation rate at 50 m at Station I might beoverestimated if other processes besides net sinkingare in play. Traps positioned in the middle of a bloom,particularly in a mixed layer, could receive particlesfrom below the trap via processes similar to resuspen-sion of particles from sediments. However, we thinkthis was not a dominant process in this case as the 50 mtrap was located in water which was stratified, albeitweakly (average Ao, [0-50 mj = 0.17).

Compared to suspended matter, chl a/POC ratios insedimented material were low (Table 4), particularly intraps at 100 m depth. Only in the 50 m trap at Station Iwas chlorophyll a the predominant pigment. Ourinterpretation is that viable Phaeocystis pouchetii cellsare the main source of sedimentation at this depth. Thepigment ratios in faecal pellets from isolated macrozoo-plankton individuals indicate'that grazing may repre-sent an important pigment loss from the upper layers ofthe Barents Sea during spring. The phytoplankton pig-ments found in the traps are, therefore, interpreted as acombination of pigment sinking in association withintact phytoplankton cells and undegraded pigmentspresent in macrozooplankton faecal pellets. Chl a-spetific Pmu values were ca 50 % of the typical valuesfor phytoplankton in the Barents Sea (Key et al. 1987).

Undegraded carotenoids are found in copepod guts(Keppel 1988) and faecal pellets (Nelson 1989, Roy etal. 1989). The same is true for accessory chlorophylls(Vemet & Lorenzen 1987). Degraded forms ofcarotenoids ate also produced by macrozooplankton(Repeta & Gagosian 1982), but mainly by larger formssuch as euphausiids and salps (Nelson 1989). Thesedegraded forms were not abundant In this study, prob-ably due to high sedimentation rates of viable phyto-plankton and the copepod dominance of macrozoo-plankton in the Barents Sea (Zenldevitch 1963, Tande& BAmstedt 1985, Skjoldal et al. 1987).

The flux of pigments as a percentage of integratedwater column values are similar to those for POC andPON (Table 2) suggesting that pigments can be used toestimate losses of phytoplankton carbon in the BarentsSea. Several studies have pointed out that low con-centrations of chlorophyll A and phaeopigments incopepods is due to transformation during gut passage,which renders them undetectable by standard methodsof pigment analysis (Wang & Conover 1986, Lopez et

192 Mar. Ecol. Pt.-ig. Ser. 66: 183-195, 1990

al. 1988). The similar percent loss of pigments, F>OCand PON indicates a dominance of ungrazed phyio-plankton sinking and/or a conservation of chlorophyllequivalents (chlorophyll a + phaeopigments) duringgut passage.

Plankton dynamics during Phaeocystlsblooms

At both stations zooplankton had little apparentinfluence on recycling of material from the Phaeocystj'spouchetii bloom in the upper 50m, coinciding wuhmassive flux of biogenic particulates from the aphoticzone (Table 3). The resulting nutrient depletion of theeuphotic zone following P. pouchetii blooms is t^iussubstantial, especially in the stratified waters of themarginal ice zone and the Polar Front represented byStation II. Even at Station I, where zooplankton grazingwas observed (H. R. Skjoldal pers. comm.), grarrrswere not able to cope with the rapid phytoplankionproduction in May/June (ca 1.5 g C m~2 d"1; F. Royunpubl.J. Sedimentation of POC comprised between 36and 58 % of primary production. At Station II, POCsedimentation comprised only 3 to 10 % of primaryproduction.

The high vertical flux rates during Phaeoo-xrispouchetii blooms have considerable implications forthe plankton ecology of the Barents Sea. Largeamounts of nitrogen and phosphorus compounds areremoved from the euphotic zone by P. pouchetii col-onies, resulting in a rapidly developing nutrient deple-tion during early summer. This rapid and exlensjveremoval of food and nutrients from the euphotic zvmegives rise to a deterioration of living conditions ofzooplankton in surface waters of the Barents Sea alttrthe spring bloom.

The lag time between phyloplankton and zooplank-ton development can be substantial in the Barents Sea{Skjoldal et al. 1987). This has obvious implications forzooplankton production and pelagic -benthic. coupling(Wassraann 1989). The evidence presented here andearlier (Bobrov 1985, Eilertsen et aL 1989, Skjoldal &Rey 1989) implies that the zooplankton community inthe Barents Sea, in contrast to other oceanic environ-ments like the North Pacific (Frost et al. 1983} and theNorwegian Sea (Peinert et al. 1989), is usually not ableto control the phytoplankton spring bloom.

Pbaeocystis pouchetii and marine snow formation

Exponentially growing PAaeocystis pouchetii col-onies are free from surface bacteria due to a moderateantibacterial property of their mucilage (acrylic acid)

(Sieburth 1979). The extracellular polymeric material ofaged P. pouchetii colonies, however, gives rise to adhe-sive webs and sticky capsular secretions which areeasily colonised by bacteria (F. Thingstad unpubl.) andpennate diatoms (Estep et al. 1990) during senescence.The stickiness of P. pouchetii colonies is important forthe biologically enhanced physical aggregation duringvertical transport fJackson 1990) which in turn givesrise to macroaggregates (marine snow) (Alldredge &Silver 1988). These aggregates sink and also removeother particles (e.g. algae, faecal pellets, detritus) fromthe upper layers as indicated by the results of thepresent study and visual observations from the bottomof the North Sea (U. Riebesell pers. comm.). Marinesnow formation enhances the depletion of participateand dissolved matter from surface water. The export ofdissolved organic carbon by P. pouchetii to the aphoticzone may also be an important mechanism for remove!of COa from the atmosphere (Toggweiler 1989). \Vehypothesise that P. pouchetii is a significant contributorto the formation of marine snow in polar and borealoceans. This is an important, but inadequately studied,aspect of its ecology.

Aulolysis, production of exudates, bacterial colonisa-tion of sinking colonies and amorphous material duringPhaeocystis pouchetii blooms (Batje & Michaelis 1986,Davidson & Merchant 1987, Vaque et al. 1989) andingestion of bacteria-rich aggregates by copepods(Estep et al. 1990) suggest that particulate and dis-solved organic matter derived from P. pouchetii bloomsis effectively recycled below the euphotic zone. This isdearly reflected by the vertical decrease in sedimenta-tion at Station I and the accumulation of ammonium inthe 50 to 100 m depth interval. Colonies of P. pouchetiialso contributed significantly to a phytoplankton sum-mer bloom in the Weddel Sea and a north Norwegianfjord, but their contribution to vertical flux at respec-tively 80 and 20 m depth and below was small(Bodungen et al. 1988, Lutter et al. 1989). It is, thus,unlikely that major amounts of P. pouchetii biomassreach the benthos of the central Barents Sea. Theimplied degradation of large amounts of the P.pouchetii derived material in the upper part of theaphotic zone means that, while sedimentation played asignificant role in the removal of P. pouchetii from theeuphotic zone, relatively little of this material is beingdelivered to greater depths. Degradation greatlydiminishes the likely importance of P. pouchetii bloomsin processes such as carbon flux to the deep ocean andsequestering of CO2. Observations of CO2 concen-trations in the water column are not available from ourinvestigation. However, storage of CC>2 at mid-waterdepths of the Barents Sea is likely during spring andsummer. This CO2 will most probably be released tothe atmosphere during winter mixing.

Wassxtnn et aJ.: Mass sedimentation of Phaeocystis pouchetii 193

We suggest the following sequence of events duringP. pouchetii blooms in the Barents Sea: (1) Flagellatedcells develop into colonies. Antibacterial substanceskeep surface mucilage free from bacteria. (2) Coloniesgrow. Nutrient depletion induces increased extracellu-lar mucilage production. Stickiness of coloniesincreases. Bacteria colonise the surface mucilage. (3)Aggregate formation of colonies and detrital materialstarts. Marine snow sinks out of the euphotic zone.Autolysis, leakage, rapid microbial degradation azidzooplankton grazing take place. (4) Marine snow disin-tegrates in upper part of the aphou'c zone.

Acknowledgements. H. C. Eilertsen, K. Estep, E. Sakshaug. F.Thingstad and K. Tande provided cozunents on the mairj-script. P.W. was supported by the Norwegian Research Coun-cil for Science and the Humanities (XA\T). M.V. and B.G.M.were supported by National Science Foundation, Division ofPolai Programs grant DPP-8520848 to O. Holm-Hansen. Wethank U. Bimstedt and H. R. Skjoldel for zooplankton samp-les, M. Hagebo for nutrient analysis. Geir Johnsen for pigme:itanalyses, C. Hewes for use of data and the crew of RV G- O.Sais' for a successful cruise. This publication is a contributionfrom the Norwegian Research Programme for Arctic Ecology(PRO MARE). We thank our colleagues in PRO MARE for thesplendid collaboration.

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This article was submitted to the editor Manuscript first received: January 3, 1990Revised version accepted: June 19. 1990