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32(l), 1987,l3l-142 Limnol. Oceanogr., Inc. @ 1987,by the Amcrican SocietyofLimnology and OccanoS;raphy, Accumulation of Th, Pb, U, and Ra in marine phytoplankton and its geochemicalsignificancet N. S. Frsfter2and J.-L. TeyssiE International I"aboratory of Marine Radioactivity, Mus6e Oceanographique, MC 98000 Monaco S. Krishnaswami and M. Baskaran Physical ResearchLaboratory, Ahmedabad 380009 India Abstract The bioaccumulation of U, Th, Ra, and Pb in four diverse nanoplanktoais algal species and a picoplanktonic blue-green alga was determined with radiotracers. Among the nanoplankton, diflerences of l-2 orderi of magnitude in volume/volume concentration factors (V'CFs) were observed for a given nuclide, but larger diferences were observed among the four nuclides, with VCF values of Th > Pb > Ra = U. The picoplanlcon cells, with greater surface: volume ratios, had significantly higher VCF values. The mean VCF values in the nanoplankton of Th and Pb were 1.5 x 105and 3.[xlOaintheliehtand2.8xlOsandT.3xl0linthedark.TheVCFsofThandPbinthe 22tTh and picoplankton were both about 2 x 106, irrespective of light. Retention half-times of iropf io fecal pellets of Artemia salina, fed radiolabeled diatoms, were 20-50 d, but >120 d for 22tTh at 4"C. ihe results suggestthat sinking plankton and their debris could a@ount for most of the natural series radionuclides sedimenting out ofoceanic surfacc waters. It is well established that several natural radionuclides, 234Th,228Th,2r0Pb,and 2r0Po, have very short residencetimes in oceanic surfacewaters (Cochran |982;Broecker and Peng 1982).The rapid removal of thesenuclides has led to the suggestionthat they are transported from surface to deep waters through biologically mediated processes (Rama et al. 1961; Bhat et al. 1969;Broecker et al. t973;Matsumoto 1975).The recent observations that the fluctuations in the settling fluxes of 228Thin the deep waters of the SargassoSea (Bacon et al. 1985) are strongly correlated with the primary productivity in the euphotic zone and that the scavenging rate of 234This proportional to primary production in the California Current (Coaleand Bruland 1985)support these earlier suggestions. However, direct mea"net surementsof Th isotopesand 2roPbin plankton" yielded low concentrations of these nuclides in this material, leading to the suggestion that biological uptake may be unimportant in the transport of these nuclides from surface to deep waters of the 'Supported in part by IAEA Contract 3209 to the Physical Researchl,aboratory, Ahmedabad, India. 2 Presentaddress:OceanographicSciencesDivision, Brookhaven National Laboratory, Upton, New York tt973. open ocean(Krishnaswami et al. 1976;Nozaki and Tsunogai 1976; Turekian 1977). We have examined this problem in more detail, since critical evaluation of the role of marine organisms in mediating the distribution of these nuclides in surfacewaters requires knowledge of their concentration in the primary producers. The net planllon used for calculating the export fluxes ofthese nuclides out of the euphotic zone would be dominated by zooplanklon and larger phytoplankton and hence would not be representative of the preponderance of marine phytoplankton. However, collection of sufficient quantities of pure phytoplankton from natural waters for radiochemical analysis is difficult. We therefore approachedthe problem by experimentally studying the accumulation of U-Th series nuclides in different species of marine phytoplankton maintained in laboratory cultures. We have included Synechococcw sp., a picoplanktonic cyanophyte. The picoplankton, relatively little studied to date, have been shown to be an'important component of phytoplanklon communities (Platt et al. 1983)and may significantly influence the movement ofparticle reactive metals in oceanic surface waters (Fisher 1985). We thank R. Anderson, M. Bacon, J. Cochran, D. DeMaster, S. Heussner,and P. 131 r32 Fisher et al. Santschi for comments on an early draft of this paper. R. Rengarajan and N. Hussain helped with computer programming. Materials and methods Experiments assessingthe accumulation of lJ, Th, Ra, and Pb in algal cultures used the centric marine diatom Thalassiosira pseudonana (clone 3H), the chlorophyte Dunaliella tertiolecta (clone Dun), the coccolithophore Emiliania huxleyi (clone MCH No. l), the filamentous cyanophyte OscilIatoria woronichinii (clone Osc N4), and the picoplanktonic cyanophyte Synechococcus sp. (clone Ll6O2). Cell dimensions, experimental procedures for media preparation, sampling, and isotope handling are all described elsewhere(Fisher etal. I983a; Fisher 1985). Cultures were incubated in constant light or constant darkness. Two' replicate cultures (three replicates for clone Ll602) and appropriate controls, with no cells, were examined for each treatment. Volume/volume concentration factors (VCFs) were calculated(Fisheret al. 1983a) for all nuclides and algal species at each sample time. The activity per cell volume was calculated by subtracting appropriate control filter values (from uninoculated "cultures") from the measuredfilterable activities in the inoculated samples.The Synechococcussp. culture was axenic, but the other cultures had some bacterial contamination as indicated by epifluorescencemicroscopy. However, in none of the cultures did the bacterial biomass exceeda few percent of the algal biomass. Moreover, most of thesebacteria passthrough the 1-g.mNuclepore filters used to filter the nanoplankton. Interference from multiple gamma emissions during measurementswas minimized by conducting experiments with either a single tracer [232Uin equilibrium with its daughters (seeFig. /), or ztoPbl or a double tracer (2toPb and 228Ra)per culture. All tracers were added as nitrates. No attempts were made to determine the speciation of the tracers after their introduction to the seawater. The time-zero water concentrations in different experiments ranged between:232U,1.2 and 11 pM (0.23-2.1Bq and 0.8 pM (0.6-5.7Bq ml-t); 228Th,0.085 0.43 pM (1 Bq ml-t); ttoPb, ml-t); 228Ra, 15 pM (10 Bq ml-t). Surfaceseawaterconcentrations of U are about 10apM, of Th <0.3 pM, of Ra about 2 x l0-o pM, and of Pb about 100 pM (Cochran 1982; Bruland 1983). The 232U'and 2r0Pbwere obtained from the C.E.A., Gif-sur-Yvette, was milked {iom 232Th France,and the 228Ra and was provided by R. Bojanowski. The pH of the cultures immediately after tracer addition was between7 .4 and 8.0. An additional experiment was conducted to measure the retention of Th and Pb in zooplankton fecal pellets. Several hundred brine shrimp (Artemia salina\ were fed dia"double-latoms (clone 3H) that had been 228Th 2toPb for 3 d and then and beled" with resuspendedinto unlabeled filtered seawater (Fisher etal.1983a). After 6 h of feeding on a suspensionof 2 x 105cells ml-r, the animals were transferred to a liter of unlabeled filtered seawatercontained in a modified fecal pellet collector (La Rosa 1976). The average fecal pellet produced was 361195 pm long and 148+35 s.m in diameter (measurementsof 80 pellets). The pellets were gently collected by largebore pipet and placed on a 43-pm nylon mesh fixed to the bottom of a polyethylene tube of 1-cm length and diameter. The polyethylene capsulecontaining the pellets (50100 pellets per capsule) was then sealed at the top with 43-pm nylon mesh. Twenty such capsules were made and assayed for their 46 keV radiation from 2toPb within about 2 h ofcollection. Three ofthe capsules were preserved as controls in a counting tube, and the remainingcapsules were held immersed in filtered seawatercontained in a glass beaker at 4"C+ 1o or 14oC+1ofor various periods up to 120 d. The water in the beaker was changed at intervals of 1-3 d. The nuclide retention was measured followingtwo approaches.In the first, a marked capsule from the set was taken out of suspension at frequent intervals, assayedfor its 2toPbactivity, and resuspendedin fresh, filtered seawater.In the secondapproach, one of the capsuleswas taken out of suspension permanently at defined intervals. This capsule was immediately assayedfor its 2r0Pb activity and after a few months for its 228Th activitv. 133 Th, Pb, U, and Ra in algae I zovr I I rstvr Fig. l. I I :.uo I -P;l -ffi1'-*J I to.on| | | oomtn | staore I 2!2Udecay series.Nuclides with half-lives > I h are shown. The concentrations ofradionuclides in all samples(i.e. water, filters,andArtemiafecal pellets)were measuredby alpha and gamma spectrometric methods. 232U'was measured by alpha spectrometry with 238U:as tracer. IJranium was separated from the samples and purified by standard ion exchangeprocedures, electro-deposited, and measured with a solid-statedetector(Bhat et al. 1969). ""Th, ttoPb, and 228Rawere measuredby nondestructive gamma ray spectrometry. 228Thwas determined by counting its progeny, 2t2Pb(22U260 ke$, to avoidthe timeconsuming analytical separations for puri228Th. The intermediate daughters fuing between 228Thand 2r2Pbare all short-lived, except fbr 224Rawhich has a half-life of 3.64 d (Fig. 1). The gowth of 2t2PbIiom 228Th would be governed by the Bateman equation (Friedlander et al. 1966) and to a large extent dictated by the half-life of 22aRa.The 2r2Pband 228Thactivities would nearly attain radioactive equilibrium after about 56 half-lives of 22aRa(around 20 d) and the 2t2Pbactivity of the sample after this period would be nearly the same as that of 228Th. (This approach would not be valid if the uptake of Ra in the cultures exceededthat of Th, although none of our samples falls in this category.) We counted the samplesperiodically over 15-20 d and calculated the 228Thand 22aRa activities in the samplesat the time of their filtration by analyzing ztzpb time-series count rates with the Bateman equation. The calculations assume that there is no loss of 22oRnfrom the samples. The observation that in each of the 2O time-zero samplesthe 2t2Pb count rate remained nearly constant (C.V. : 3-7o/o)throughout the 20-d counting period suggeststhat 22oRnloss from the sampleswas negligible. 2toPbwas measured by counting its 46 keV photon emissions (35-55 keV) and 228Ravia the photons of its daughter 228Ac(865-1,010 keV). The 228Rasampleswere countedl-Z d after their filtration to ensure radioactive equilibrium between228Raand 228Ac(t,^: 6.1 h). All phytoplankron samples were counted with a Packard 5650 Autogamma counter [with a NaI(T1) crystall under identical counting conditions. The 228Thassay (via 2t2Pb)in the fecal pellets was performed with an Ortec intrinsic gamma-X germanium detector. Whenever a double tracer was used, necessarycorrections for interference in the peak regions were made by counting appropriate standards. Results The growth of the cells and their accumulation of 228Thand 2r0Pbare shown in Figs. 2 and 3. The uptake of 232U'and228Ra by the phytoplankton was extremely low (<2o/o of the activity in the water column, throughout the course of the experiments). The fractions of filterable radionuclide in the uninoculated control sampleswere very low (< lolo)for all nuclides except 228Th,for which it averagedabout 230lowith the nanoplankton experiments and < 100/owith the picoplankton experiment (Figs. 2, 3). Equilibrium with respect to fractionation between the dissolved and the particulate phases of the radionuclides was generally achieved in 1 d. The nuclide concentration per cell at 1 d was generally within a factor of two of its value after a 3-d exposure for all isotopes and algal speciesexcept for the 2roPbcontents per 3H cell in the light after a 3-d exposure, where it was 5-6 times lower than those after exposurefor I d. This observation probably resulted from a cell division rate of 3H that exceededthe 2roPb adsorption rate. Thus, the VCF values did not change appreciably after I d, except for 2toPbin illuminated 3H cells (Figs. 2, 3). Generally, algal uptake followed the pattern 228Th;, zropf 2 z3zlJ - 228Ra.Concentration factors after exposurefor 3-6 d are given in Table 1. The differencesbetween the VCF values.for the different algal species Fisher et al. t34 log cells ml-1 228Th uptake log VCF 3H A Dun | ----4 { Mch 4 Osc 4 Syn 5 DAYS DAYS 2 DAYS Fig.2. Growth of cells (3H: Thalassiosirapseudonana;Dvn: Dunaliella tertiolecta;Mch: Emiliania huxleyi; 22tTh under light (a) and dark (O) Osc;-Oscillatoria woronichinii; Syn: Synechococcussp.) and accumulation of 22tThcaughton a I -pm Nuclepore 22ETh percent water column of the uptake representsthe conditions. The percent filter (0.2-pm filier for Syn). 22tThuptake by control filters (from uninoculated water) shown with solid symbols; 22tThVCF values take into account the 22EThcontent of controls for 3H, Dun, Mih, and Oic identical. The blank (control) filters. Data points are means + I SD of two replicate cultures (three replicatesfor Syn). r35 Th, Pb, U, and Ra in algae log cells ml-1 21o Pb uptake log VCF (%) 1 : 3H 5 5 \ 4 6 4 6 Dun 5 4 6 Mch DAYS Fig. 3. As Fig. 2, but of 2toPb. Fisher et al. 136 o) .g o E o (I (D 10 = €(U ro 4"C 14"c 0 1m 110 DAYS 22sTh 2roPb (!, (O, O) and Fig. 4. Retention of ) by Artemia salina feeal pellets maintained in unlabeled seawaterat 4"C and l4qc. for any one nuclide were smaller than the differencesamong the nuclides for any one species.The highest VCF value measured was -2 x 106fbr 228Thand 2r0Pbin Synechococcussp. (Table 1). The VCF values for 2roPband 228Thin algaeincubated under light and dark conditions were generally similar (Table 1; Figs. 2, 3). In the illuminated D. tertiolecta and O. woronichinii cultures, pH increasedconsiderably as the cells divided, going from about 7.9 after I d to about 9.0 after 3 d. Since the VCF values for 2r0Pband 228Thin light and dark cultures were similar (Table 1), this pH increase apparently had no major effect on nuclide uptake by these species. The retention of 2r0Pbin A. salina fecal pellets contained in the repeatedly sampled capsulesis shown in Fig. 4. Both at 4oCand 14'C, -90o/o of the 2toPbin the pellets is lost within 120 d. The loss curve at 4oCis nearly exponential \Mith a single rate constant,which yields a retention half-time (rbu,) of 36+3 d fbr 2toPbin the pellets.The loss curve at I4"C seems to show two components, characteized by a rapid loss during the initial stages(tb*: 10+0 d) followed by a more gradual loss (lbu,: 32+4 d). If we combine the 2r0Pbloss data from different capsulesfor the same temperature and time, the loss curves show greater scatter; the tbv,values for the pooled data are then 45+6 d at 4oC and 23+2 d at 14'C. The fecal pellets retained 228Thmore than ttoPb, as there was no discernible loss of 228That 4"C, while atl4"Cthetbr,was30-44 d. The differential retention of 228Thand 2r0Pbin fecal pellets held at 4"C suggeststhat physical breakup of the pellets was not solely responsible for the measured loss of radionuclides (at least at 4"C). Discussion The concentration factors of the nuclides in the algal species studied generally followed the trend Th > Pb > Ra = IJ. Comparison of the concentration factors with those measured for transuranic elements in these cells (Fisher et al. 1983a; Fisher and Fowler in press) shows that the accumulation of Th is similar to the particle-reactive elementsAm, Pu, Cm, and Cf. The minor influence of light on the accumulation of U-Th series nuclides in these species was similar to earlier findings for other metals by Fisher et al. (1983a, 1984) and Fisher (1985).Theseearlier studiesconcludedthat metal association with phytoplankton proceeds by adsorption to cell surfaces. Lead 137 Th, Pb, U, and Ra in algae Table l. Volume/volum€ concentration factors (VCFs) obtained from phytoplanlton in culture. Means + I SD, rz: 2 for all cellsexceptLI602 {n : 3)' (Not determined-nd.) Clone Condilion 22rThr 39+ll 106+23 3H (diatom) Light Dark Dun (green) Light Dark 4l+7 5 7+ 7 Mch (coccolithophore) LiCht Dark 3l+12 49+23 Osc (blue-green) Light Dark 1.1+0.7 2 . 1 +l . l Lr602 Light Dark l90r l2t r99+24t (blue-green) 'roPbt 3.7+0.4 4 7+ 6 l0r4 6.3+2 3.4+0.6 4.7+0.9 1.3+0.2 1.9+0.6 264+61 178+46 2!2(J* <0.02 <0.06 <0.04 <0.02 <0.01 <0.06 <0.004 <0.002 nd nd ,rRa+ <0.03 nd nd nd <0.03 nd <0.006 nd nd nd * Equilibration time of 96 h. f Equilibration time of 70 h. * Equilibration timc of 144 h. and americium have been shown to associate principally with the cell walls of marine phytoplankters (Fisher et al. 1983c), and presumably other particle-reactive, nonessential metals like Th would do the same. The high affinity of Pb and especially Th for phyoplankton suggeststhat they are particle-reactive in general, consistent with their known marine geochemical behavior and their long retention in Artemia fecal pellets. The association of Th with marine particulate matter has been shown to be reversible and in equilibrium with adsorption/desorption processes (Nozaki et al. 1981;Bacon and Anderson 1982).In open ocean waters, the residencetimes of Th isotopes in marine suspendedmatter have been calculatedto be in the rangeof 2-10 rnonths (correspondingto a tb^of about 45-200 d), based on vertical profiles of dissolved Th isotopes in open oceanwaters (Nozaki et al. l98l; Bacon and Anderson 1982). We have observed that the tb* of 228Th in Artemia fecal pelletsheld at 4C is > 120 d. The retention of 2roPband 228Thin the fecal pellets was comparable to that of 24rAm-a particle-reactivetransuranic nuclide-in euphausiid fecal pellets (Fisher et al. 1983b).The scatterin the 2roPbretention data derived from different fecal pellets (i.e. different capsules) probably was more a function of different physical characteristics, including degradation rates, among the different batches of pellets than of varia- tions in the desorption rates for the nuclides. The influence of biological and physical degradation of the fecal pellets, if any, on retention of radionuclides warrants further study. It can be surmised from our data that the desorption of these elements from sinking fecal pellets would proceed slowly in nature, and fast-sinking fecal pelletswould be expectedto transport theseelements,like the particle-reactive transuranic elements, to deep waters and sediments (Higgo et al. 1977;Fisher and Fowler in press).Consistent with this idea, Coale and Bruland (1985) concluded that zooplankton fecal pellets were responsible for the transport of Th in the California current. Table 2 presents a comparison of concentration factors of Th, Pb, Ra, and U in the phytoplankton cultures with those in various types of suspended particulates in seawater. Concentration factors were also calculated on dry weight bases(DWCFs) to facilitate comparisons with available field data. The geometric mean DWCFs in the phytoplankton cultures studied here are 8.7 x 105for Th and 2.9 x 105for,Pb. If we exclude the D. tertiolecta and O. woronichinii data to avoid any possible pH artifacts, thesegeometric means are not altered appreciably (in fact, they increase about twofold). The geometric mean DWCFs in phytoplankton cultures are comparable to those measured in surface ocean particulates and in sediment trap materials (Table 2). Field data of Krishnaswami et al. (1976) Fisher et al. 138 Table 2. Comparison of dry weight concentration factors (DWCFs) obtained from laboratory culture experiments with those determined from measurementsof marine particulate matter. DWCF (x l0') Algal cultures T. pseudonana D. tertiolecta E. huxleyi O. woronichinii Synechococcussp. Surfacewater particles Atlantic Ocean Indian Ocean GeosecsNo. 48, S. Atlantic Deep water particles Panama and Guatemala basins Sediment trap material N. Atlantic (389 m) N. Atlantic (1,000m) Net plankton Phytoplankton Phytoplankton Mixed plankton Mixed plankton Zooplanhon (copepodsand crab larvae) Zooplankton (salps) Zooplanhon (calanoidsand cyclopoids) 106 244 89 2.2 975 l0 60 l0 3 1,100 <0.08 <0.09 <0.01 <0.06 <0.2 <0.03 <0.008 2 200 80 Krishnaswami et al. 1976 Krishnaqwamiet al. l98l Somayajulu and Craig 1976 l0 2,000 200 450 Bacon and Anderson 1982 50 100 : 0.6 2 Present work Present work Present work Present work Present work 3 7 Brewer et al. 1980 Brewer et al. 1980 z;a - 0.18 0.7 0.12 Shannonet al. 1970 Shannon and Cherry l97l Szabo 1967 Knauss and Ku 1983 0.01 0.03 Krishnaswami et al. 1985 Krishnaswami et al. 1985 0.02 Kharkar et al. 1976 0.2 l indicate that 23aThconcentration factors in marine particulate matter decreasewith increasing suspendedparticulate load. Since the particulate load in ourexperiments (>0.3 mg liter-t) exceededthat of all but the most productive waters, it may be expected that the measured concentration factors (and subsequent flux estimates) in the phytoplankton culturesrepresentlower limits. The high concentration factors of Th and Pb in phytoplankton suggestthat these organisms could be important sequesteringagents for thesenuclides in surfacewaters and that the flux of organic material out of euphotic waters, either by direct sinking of phytoplankton cells or packagedinto zooplankton fecal pellets, could appreciably influence the vertical flux of these nuclides. Table 3 presents a range of estimates of organic carbon exported from the euphotic zones of different oceans together with an estimate,basedon mean DWCFs ofTh and Pb derived in our laboratory experiments, 0.05 0.05 0.5 of the flux of 234Thand 2roPb associated with sinking phytoplanl<ton (in whatever form). The flux of radionuclides should be a function of the sinking particulate load, which is in turn a function of the primary production in the euphotic zone (Honjo 1982;Deuseret al. 1983;Jickellset al. I 984), provided that the radionuclide: C ratios in the primary producers and settling organic matter are identical. However, if the radionuclides are not recycled in surface waters as efficiently as carbon, then the nuclide fluxes presentedin Table 3 would be lower Iimits. The estimates of 234Thand 2roPb fluxes on an oceanwide basis via sinking phytoplankton (Table 3) can be compared with the measured fluxes of these nuclides from the euphotic zone. Data on the 23aThremoval rate from surface waters are obtained from 234Th' 238U' ratios. On the basis of a mean value of 0.8 for the 234Th' 238U.activity ratio in surface waters (- 100 m) of the mid-Arabian Sea, Th, Pb, U, and Ra in algae Wharton Sea, and North Pacific, the 234Th removal is calculatedto be -50 x 10adpm m-t yr-t (Bhat et al. 1969; Matsumoto 1975). For oligotrophic waters such as the SargassoSea,an estimateof 234Thremoval can be obtained from 228Thdata. The residencetimes of 228Thare (6 yr in the upper 100 m of these waters and <29 yr in the upper 350 m, correspondingtoremoval rate constantsof >0.167 yr-t and >0.035 yr-t (Li et al. 1980).If we assumethat 234Thand 228Thhave the same residencetime (Kaufman et al. 1981) and a234Thstanding crop of 2 x 105 dpm --z (at 100 m), then the 234Thremoval flux can be calculated to be 0.7 to 3.3 x 104dpm 6-zy1-t. We estimate the removal flux of 234Thin oligotrophic watersvia sinking phytoplankton to be l.l x l0a dpm m-2 yr-t, using a new production rate of I.54 gC m-2yr-r (Eppleyand Peterson 1979) and the mean DWCF of 8.7 x 105in phytoplankton cultures. For waters of high productivity such as in the Antarctic, there are no water-column data for calculating the 234Thremoval flux, although an upper limit can be set by assuming the removal rate = production from 139 Table 3. Estimates of fluxes of 234Thand 2'0Pbinfluencedby phytoplankton in different waters. Flux from the euphotic zone Org. C' GCm-' yr-') Atlantic 27 Pacific 8 Indian 18 Arctic 0 Antarctic 146 Flux at - 100 m :r.Tht ( x 1 0 .d p m m-2 yr-r) 18.8 5.6 t2.5 0 r02 O.z-3.3$; 50ll ir0Pb+ ( x 1 0 3d p m m-2yr-r) 6.3 1.9 4.2 U 33.9 5-20# t Assumesequalto "new" primary production(from EppleyandPctcrson 1979). t Using geomerric mean DWCF of 8.7 x I 0t (Table 2) and surfacewater 2r"I'hof 2 dpm liter-r(Coalcand Bruland 1985);assumes C:0.25 dry wt. x gcometric (Tablc mean DWCF of 2.9 lOt 2) and surfacewater * Using 2roPbconcentrationof 0.2 dpm liter-r (Cochran 1982);assumcsC wt. 0.25 dry 0 For oligotrophicwaterssuchas the SargassoSea(from Li ct al. I 980); assumes2!'Th and 22rThrcmoval rale constantsarc equal (Kaufman e rs l . l 9 8 l ) . ll Calculatcdfrom Bhat et al. 1969 and Matsumoto 1975. # From Bacon.l al. 1976and Nozaki and Tsunogai 1976. parison of measured 234Thfluxes at specific oceanic sites with fluxes predicted for these waters using our laboratory-derived concentration factors and available data on new production rates shows good agreement.For 238U'ry 200 x 104 dpm p-zy1-t. For 2t0Pb, example,in the California Current (36o50'N, x 123"00'W; MLML Pit Cruise-2) our data the removal flux is about 5-20 103dpm sl-z y1-t (Table 3). A major problem asso- would predict a removal flux of 8 x 105 ciated with calculating 2r0Pb removal flux dpm m-2 yr-r for a new production rate of is the paucity of data on its atmospheric I l6 g C m-2yr-'(Coale and Bruland 1985). deposition. When estimated234Thand 2roPb This estimate compares with the value of removal fluxes via phytoplankton are com- -7.3 x 105dpm 6-z y1-t basedon water pared with those calculated from their sur- column inventories and sediment trap flux face water (-100 m) inventories, both in of 234Th(Coale and Bruland 1985). Simioligotrophic waters (suchas the central sub- larly in the VERTEX-I station (36'36'N, 123%8'W) our data would predict a 234Th tropical regions) and in hiehly productive (e.g. waters upwelling regions,neritic waters, removal flux of 5.7 x 105dpm m-2yr-r for Antarctic waters), we find that > 500/oof the a new production rate of 82 g C rys-zy1-t 234Thsedimenting out at 100 m probably is (Knauer et al. 1984). The 234Thflux at this associated with the phytoplankton or their location basedon its deficiency in the water debris. Further, the estimates in Table 3 column is 5.5 x 105dpm m-2 yr-t (Coale show that the phytoplankton and their de- and Bruland I 985). For 2r0Pba similar combris could be a significant pathway for re- parison can be made for the MLML Pit moving 234Thand 2r0Pbfrom surface ocean Cruise-2station.Basedon a DWCFof2.9 x waters. 105,a new production rate of 116 g C m-2 yr-r, and a 2roPbconcentration of 0.2 dpm Support for these suggestionscomes from (Bacon studies et al. 1985; Coale and Bru- liter-r, we would predict a removal flux of land 1985) showing positive correlations 2.7 x L04dpm m-2yr-t. The measuredflux between 228Thand 234Thfluxes and primary at this station is 1.9 x lOa dpm 6-z y1-t production in various surface waters of the (Coaleand Bruland 1985). North Atlantic and the North Pacific. ComIn light of these findings, the suggestions 140 Fisher et al. of Nozaki and Tsunogai (1976) and Tur- highly calcified macroalgae, presumably by ekian (1977)that biologicalremoval of 2toPb coprecipitation with the calcium carbonate matrix (Edgingtonet al. 1970).However, in and 23aThwould account only for a minor fraction of their flux from surface waters our study no pronounced differences were need re-evaluation. The lower 2r0Pb and observed between the concentration of Ra 234Thenrichment factors these workers re- in the coccolithophore,E.huxleyi and in the ported for plankton probably result from noncalcareous phytoplankton. Analogous measurementsof comparatively large, net to Ra, the distribution of Ba in the sea applankton, dominated by zooplankton. We pears to be linked to that of Si (Li et al. would speculate that particle-reactive ele- 1973; Collier and Edmond 1984). As with ments like Th and Pb should show a direct Ra, the major siliceouscarrier phasefor Ba correlation between enrichment factors and hasnotbeen identified @ankston etal.1979; surface: volurne ratio of the particles (or or- Collier and Edmond 1984). It is likely that ganisms),as seenfor Am, Cm, Pu, and Cf the cycling of Ra and Ba are governed by (Fisher and Fowler in press), thereby re- the same process(es),such as the biologisulting in higher concentration factors in the cally mediated formation of barite crystals smaller phytoplankton than in the larger in the water column (Dehairs et al. 1980). phytoplankton and the zooplankton. The The low concentration of U in the phydata for Th and Pb (this paper) and other toplankton may be a result of the speciametals (Fisher 1985) in the picoplankton tion of U in an anionic complexfurther support this idea. The data of Shan- UOr(CO3)ro- -in seawater (Stumm and non et al. (1970)on 2r0Pbin net phytoplank- Brauner 1975).This complex may be genton yield a DWCF of I x 105,comparable erally unreactive for suspendedmarine parto the mean value based on our experi- ticulates (such as phytoplankton) which carments. It is recognized,however, that there ry a negative surface charge (Myers et al. is considerable scatter in the available field 1975; Neihof and Loeb 1972). Moreover, data. the affinity ofU for dissolved carbonate may The close similarity in the dissolved pro- greatly exceedits afrnity for ligands on algal files of 226Raand Si in the world ocean sug- surfaces. Consistent with this hypothesis, gests that 226Radistribution in the oceans algal uptake of IJ, which was attributed to is affected by the same processesthat affect U adsorption to cell surfaces,was found to the Si distribution (Ku et al. 1970, 1980; be maximal at pH 5, being markedly inhibChung 1980). Sediment trap data on the ited by the presenceofcarbonate (Sakaguchi settling fluxes of 226Raand biogenic SiO2 et al. 1978;Horikoshi et al. 1979).Analyses show a very strong positive correlation with of sediment trap samples yield a IJ concena slope of 26 dpm 226Rsg-t SiO2 (Brewer tration of about 1.1 dpm g-t dry biogenic et al. 1980). Given a typical 226Raconcen- matter (Breweret al. 1980;Anderson 1982), tration of 0.2 dpm liter-t in seawaterand a corresponding to a DWCF of about 500. biogenic SiO2 content of 50o/oin siliceous This value is consistent with the results oborganisms, the sediment trap data yield a tained from the phytoplankton cultures (TaDWCF of about 6 x 104in siliceousorgan- ble 2), suggesting that the phytoplankton isms. Attempts to identifu 225Ra-concen- uptake of U in surfacewaters could account trating organisms have thus far not been for the measured fluxes of this element successful,exceptfor the observation of high through the water column. concentrations of 226Rain Rhizosolenia sp. In summary it would appear that Th and (Shannonand Cherry I97I). Our resultson Pb are very reactive for marine particulate Ra uptake by T. pseudonana, another cen- matter, including phytoplankton and zootric diatorn, failed to show substantial plankton fecal material. Their flux from surbioaccumulation of this element. Ra has face waters should be governed by associbeen shown to be concentrated heavily by ation with the surfacesof sinking particulate zooxanthellae associated with coral reefs, matter and therefore be a function of priwith a DWCF of about 3 x 106(Flor and mary productivity in the euphotic zone. By Moore 1977).Similarly, Ra concentratesin contrast. U and Ra behave relativelv con- Th, Pb, U, and Ra in algae t4l nuclides, p. 384-430. In M. U- and Th-series servatively with respect to association with Ivanovich and R. S. Harmon [eds.], Uranium sebiogenic particulates. We note, however, ries disequilibrium - applications to environmenthat these conclusions are based on expertal problems. Oxford lJniv. Press. imental laboratory studies with only a few Collren, R., aryu J. Ept"toNp. 1984. The trace element geochemistryof marine biogenic particulate algal species.It is difficult to judge how far matter. Prog. Oceanogr.13: I l3-199. these laboratory culture experiments can be DeHerns, F., R. CnrssELET,AND J. Jnpwnn. 1980. used to predict natural marine biogeochemDiscrete suspendedparticles ofbarite and the barium cycle in the open ocean. Earth Planet' Sci. ical processes.However, the observation Ixtt. 492528-550. that our results are consistent with available W. G., P. G. Bnewen, T. D. Jlcxu.Is, nNp R. DEUsen, field data is certainly encouraging. Further F. Couumu. 1983. Biological control of the reresearchwith many more speciesand varymoval ofabiogenic particles from the surfaceocean. ing experimental conditions should help to Science219: 388-391. quantifu the role of organisms in mediating EocrNGroN, D. N., S. A. GonooN, M. M. Tnoulrars, nNp L. R. At-uopovm. 1970. The concentration the distribution of these nuclides in marine of radium, thorium, and uranium by tropical masystems. rine algae.Limnol. Oceanogr.15: 945-955. References ANoeRsoN,R. F. 1982. Concentration, vertical flux, and remineralization of particulate uranium in seawater.Geochim. Cosmochim. Aeta 46212931299. BecoH, M. P., mrp R. F. ANornsoN. 1982. Distribution ofthorium isotopesbetweendissolvedand particulate forms in the deepsea.J. Geophys.Res' 87:2045-2056. -, C.-A. HuH, A. P. Furn, lNo W. G. Deusrn. 1985. Seasonality in the flux of natural radionuclides and plutonium in the deep SaryassoSea. Deep-SeaRes. 32: 273-286. D. W. SpsNcER,AND P. G. BnewER' 1976. 2roPb/226Ra disequilibria in seaand 2r0Po/2r0Pb water and suspended particulate matter. Earth Planet. Sci. I*tt. 322277-296. AND Ber.ucsroN,D. C., N. S. Flsnrn, R. R. GurLL,c,RD, V. T. BowrN. 1979. Studiesof elementincorporation by marine phytoplankton with special referenceto barium. Environ. Meas.I-ab. Environ. Q.U.S. Dep. EnergyEML-349,p. 509-531. Bn,tr, S. G., S. KrrsxNAswAMl, D' Ler,, RAMA, ANo ratios in the W. S. Moons. 1969. 234TW238U ocean.Earth Planet. Sci. Irtt. 5: 483-491. 4. t' BnswEn,P. G., Y. NozAKl, D. W. SpeNcER,,AIID Fleen. 1980. Sediment trap experimentsin the deep North Atlantic: Isotopic and elementalfluxes.J. Mar. Res. 38: 703-728. BnoecKEn, W. S., A. K.lurrtalN, ANo R. M. Tmsn. 1973. The residencetime of Th in surfacewater and its implications regardingfate of reactive polIutants. Earth Planet. Sci. Lett. 20235-44. nNp T.-H. Pmc. 1982. Tracersin the sea. Eldigio. BnuLANo, K. W. 1983. Trace elementsin sea-water, p. 157-220. In J. P. Riley and R. Chester [eds.], Chemical oceanoglaphy,v. 8. Academic. CHUNc,Y. 1980. Radium-barium-silicacorrelations and atwo dimensional radium model forthe world ocean.Earth Planet. Sci. Lett.49: 309-318. Coar-e,K. H., ruto K. W. Bnu-aNp. 1985. 23oTh: 23sUdisequilibria within the California current. Limnol. Oceanogr. 30222-33. CocHneN. J. K. 1982. The oceanic chemistry of the Errrev, R. W., eNo B. J. PsrsRsoN. 1979. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 2822677480. FrsHrn, N. S. 1985. Accumulation of metals by marine picoplankton. Mar. Biol. 87: 137-142' P. BrennecAARD,axp S. W. Fowun. 1983a. Interactions of marine plankton with transuranic elements.l. Biokinetics of neptunium, plutonium, americium and californium in phytoplanlton' Limnol. Oceanogr.28t 432-447. marine plankton with transuranic elements. 3. Biokineticsofamericium in euphausiids'Mar. Biol. 752261-268. -r M. BoxE, erp J.-L. Teyssri. 1984. Accumulation and toxicity of Cd, Zn, Ag, and Hg in four marine phytoplankters. Mar. Ecol. Prog' Ser. 1 8 :2 0 1 - 2 1 3 . K. A. BunNs,R.D. CHennv,ANoM.HsvRAup. 1983c. Accumulation and cellular distribution of "tAm, 2r0Poand 2toPbin two marine algae'Mar. Ecol. Prog. Ser. 11: 233-237. -r eNp S. W. Fowr"en. In press. The role of biogenic debris in the vertical transport oftransuranic wastesin the sea. In T . P. O'Connor et al. [eds.], Oceanic processesin marine pollution, v. 2. Krieger. Fron, T. H., ANDW. S. Moonn. 1977. Radium/calcium and uranium/calcium determinations for westernAtlantic coral reefs,p. 555-561. InPtoc. 3rd Int. Coral Reef Symp. Miami, Fla. eNo J. M. MrLLen. FnrrDlnNpsn, G., J. W. K-EI.u.{Epv, 1966. Nuclear and radiochemistry, 2nd ed' Wiley. Hrcco, J. J., R. D. CHrnnv, M. Hrvuuo, aNp S' W. Fowrrn. 1977. Rapid removalofplutonium from the oceanicsurfacelayer by zooplankton fecalpellets. Nature 266t 623-624. HoNro, S. 1982. Seasonalityand interactionof biogenicand lithogenic particulate flux at the Panama Basin.Science218: 883-884. HomosHr, T., A. NaxllIue, exp T. Slx.ecucm. 1979. Uptake of uranium by Chlorella regularis. Agric. Biol. Chem. 43:617423. Jrcrrus, T. D., W. G. DeusEn,4ryp,A.H. KNp. 1984. The sedimentation rates of trace elementsin the t42 Fisher et al. 234Th-238{J radioactive disSargassoSea measured by sediment trap. Deep- Mnrsurraoro, E. 1975. equilibrium in the surfacelayer of the ocean.GeoS e aR e s .3 l : 1 1 6 9 - 11 7 8 . chim. Cosmochim.Acta 39:.205-212. A., Y.-H. LI, e.NoK. K. TunrrrnN. 1981. KAUFMAN, The removal rates of 23aThand 226Thfrom waters Mvrns, V. B., R. L. IwnsoN, eNo R. C. Hnnmss. 1975. The effectof salinity and dissolved organic matter of the New York Bight. Earth Planet. Sci. Lett. 54: on the surfacecharge characteristicsof some eu385-392. KHenx-m, D. P., J. THousoN, K. K. TunEruAN,AND ryhaline phytoplankton. J. Exp. Mar. Biol. Ecol. 17: 59-68. W. O. Fonsren. 1976. rJranium and thorium decayseriesnuclides in plankton from the Carib- NrrHor, R. A., nxp G. I. Lors. 1972. The surface chargeof particulate matter in seawater.Limnol. bean. Limnol. Oceanogr.2lz 294-299. Oceanogr.l7z 7-16. Krnusn, G. A., J. H. M.lnrrn, eNp D. M. I(nnr. I 984. The flux of particulate organic matter out of the Noznn, Y., Y. HoRran,eNp H. Tsusora. 198l. Water column distributions of thorium isotopes in the euphoticzone, p. 136-150. In Global oceanflux westernNorth Pacific. Earth Planet. Sci. Lett. 54: study. Workshop Proc. Natl. Acad. Sci. 203-216. Kxnuss, K., avp T.-L. Ku. 1983. The elemental er.ro S. TsuNooru. 1976, 226Ra,2r0Pband composition and decay-seriesradionuclide con- -s 2'0Podisequilibria in the western North Pacific. tent of plankton from the East Pacific. Chem. Geol. Earth. Planet. Sci. Irtt. 32t 313-321. 392125-145. KnrsrrNeswevr,S., M. BasxnnaN, S. W. Fouen, nNo Pr,err, T., D. V. Sunsn RAo, eNp B. InwrN. 1983. Photosynthesisof picoplankton in the oligotrophic M. Hevnlup. 1985. Comparativerole of salps ocean.Nature 30lz 702-704. and other zooplankton in the cycling and transport Rc,l'rl,M. Koroe, eunE. D. Gor-psenc. 1961. Leadof selectedelementsand natural radionuclides in 210 in natural waters.Science134: 98-99. the Mediterranean waters. Biogeochemistry l: 353SnmcucHr, T., T. HonrKosHI, aNp A. Nlxerurle. 360. 1978. Uptake of uranium from seawater by miD. LAL, nNp B. L. Souevalulu. 1976. Incroalgae.J. FermentationTechnol. 56: 561-565. vestigationsof gram quantities of Atlantic and PaSneNNoN,L. V., nr.ro R.D. Cnennv. 1971. Ra-226 cific surfaceparticulates. Earth Planet. Sci. ktt. in marine phytoplanl:ton. Earth Planet. Sci. ktt. 32t 403419. 1r:339-343. 1981. B. L. Souevnrulu. M. M. Se,nrr*, eNp Chemicaland radiochemical investigationsof sur210 and lead-210 in the marine environment. faceand deepparticles ofthe Indian Ocean.Earth Geochim. Cosmochim.Acta 34: 701-711. Planer.sci. I-ett. 54: 8l-96. Ku, T. L., C. A. Hua, ANo P. S. CHeN. 1980. Me- Sounvlruru, B. L., ero H. Cnarc. 1976. Particulate and soluble 2'0Pbactivities in the deep sea.Earth ridional distribution of 226Rain the easternPacific Planet. Sci. ktt. 322268-276. Planet. Sci. along GEOSECScruise tracks. Earth Sruuu, W., ANp P. A. Bn{rrrven. 1975. Chemical Iett. 492293-308. speciation,p. 113-239.In J.P. Riley and G. SkirY.-H. Lr, G. G. MenuEU, ANDH. K. Wowc. row [eds.],Chemical oceanography,v. l. Academ1970. Radium in the Indian-Antarctic Ocean ic. south of Australia. J. Geophys. Res. 75: 5286Sznso, B. J. 1967. Radium content in plankton and 5292. seawater in the Bahamas.Geochim. Cosmochim. Le Rosn, J. 1976. A simple system for recovering A c t a3 1 : l 3 2 l - 1 3 3 1 . zooplanktonic fecal pellets in quantity. Deep-Sea TuneKrAN, IC K. 1977. The fate of metals in the Res.23:995-997. oceans.Geochim. Cosmochim. Acta 4l: ll39eNo J. R. Toccwnnrn. 1980. Lr, Y.-H., H. W. FEEt-Ey, 228Raand 228Thconcentrations in GEOSECSAttt44. lantic surfacewaters. Deep-SeaRes. 27: 545-555. -, T. L. Ku, G. G. MerHrEu, A\rDIC WOT.GEMUTH. 1973. Barium in the Antarctic Oceanand impliSubmitted: 13 May 1985 cations regarding the marine geochemistryof Ba 226Ra. Accepted:20 June 1986 19: 352-358. Earth Planet. Sci Lett. and