Environ. Sci. Technol. 1997, 31, 2584-2588
Mechanism for Enhanced Uptake of Radionuclides by Zooplankton in French Polynesian Oligotrophic Waters R O S S A . J E F F R E E , * ,† FERNANDO CARVALHO,‡ SCOTT W. FOWLER,‡ AND JAIME FARBER-LORDA‡ Environment Division, Australian Nuclear Science and Technology Organisation (ANSTO), PMB 1, Menai, 2234, Australia, and IAEA Marine Environment Laboratory, P.O. Box 800, MC-98012, Principality of Monaco
A study of natural radionuclides in zooplankton collected during 1990-1992 from the low productivity waters of French Polynesia has demonstrated the presence of enhanced uptake of Po-210 by zooplankton when zooplankton biomass is low. Po-210 in zooplankton increases exponentially to previously unreported levels up to 3200 Bq/kg dry weight, as their biomasses decline to levels as low as 0.14 mg dry weight/cubic meter. A validated mathematical model, incorporating the established role of zooplankton in the removal of Po-210 from the water column, captures the shape of this empirical relationship and also explains this biomassrelated mechanism that increases Po-210 concentrations in zooplankton. Our results and analysis point to the enhanced vulnerability of such low productivity marine systems to environmental contamination following potential leakage of radionuclides from former weapons test sites and radioactive waste repositories that have been recently proposed for the Pacific.
Introduction Zooplankton are important in the dynamics and transfer of radionuclides in the marine environments (1, 2). Predominantly through production of rapidly sinking faecal pellets, which contain enhanced concentrations of radionuclides, they rapidly remove particle-reactive radionuclides including Po210 and Pb-210 from the euphotic zone (1-5) to the extent that water concentrations of the radionuclides could be reduced. The capacity of zooplankton to accumulate various radionuclides to elevated concentrations in their bodies has led to their use as biomonitors of radionuclides in French Polynesian waters in relation to nuclear weapons testing within the Mururoa and Fangataufa Atolls, Tuamotu-Gambier Archipelago (6). We report here an unusual inverse and nonlinear relationship between Po-210 concentration and biomass of zooplankton from these oligotrophic waters. Although the region is remote from continental sources of Po-210’s progenitor (Rn-222), concentrations in zooplankton are up to an order of magnitude higher than levels previously reported. A validated mathematical model, incorporating the established role of zooplankton in the removal of Po-210 * Corresponding author. † ANSTO. ‡ IAEA Marine Environment Laboratory.
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from the water column, reflects the shape of this empirical relationship and explains this biomass-related mechanism that renders Po-210 concentrations up to 3200 Bq/kg (dry weight).
Materials and Methods Zooplankton Collection and Characterization. Zooplankton were collected between August 1990 and March 1992 from French Polynesian waters within latitudes 6-28° S and longitudes 134-154° W using standardized methodologies previously detailed (6). Their biomass varied between 0.14 and 5.44 mg (dry weight)/m3, with a median zooplankton biomass of 0.8 mg (dry weight)/m3, more than 2 orders of magnitude less than the global average (7). Their sparseness is consistent with their location in a vaster area with primary productivity typically less than 50 g‚m2‚annum of biologically fixed carbon (8). Reduced Pb-210:Po-210 water concentration ratios in low productivity gyres of the Pacific are attributed to the reduced biologically-mediated rates of Po-210 removal (9), with this ratio being regarded as a good measure of relative biological productivity (10, 11). It has been common to use the reverse ratio of Po-210:Pb-210 in such studies. However we have consistently used the converse Pb-210:Po-210 ratio because its positive association with increasing productivity enhances the clarity of subsequent comparisons made in the paper. For eight samples collected from waters in the vicinity of the Marquesas Archipelago, subsamples that represented from 2 to 5% of the total sample by wet weight were taken near the time of collection and preserved in 5% formaldehyde for subsequent quantitative characterization of taxonomic composition. Preserved samples were filtered through a fine mesh, rinsed with tap water, strained, and placed in 10% ethanol. The large sample sizes were further reduced using a sample splitter for thoroughly agitated samples to reduce size-dependent centrifugal sorting with a consequent bias in the subsampling procedure (12). These subsamples were then used to characterize the major taxonomic groups present by dark field microscopy. The taxonomic composition shown is mean (n ) 8) proportional abundances of individuals occurring in each of the 10 most abundant taxonomic categories. Because percentage values are known to form a binomial distribution, an arcsin transformation [X′ ) arcsin (X)0.5] was used to generate distributions approximating normality, prior to the calculation of the mean proportional abundances (+1 SD) shown (13). The category Copepoda is composed of both Calanoida and Podoploea (12). During taxonomic characterization of individuals, inclusive of all taxonomic groups, a scaled graticule was used to assign them among six categories of maximum length to derive percentage occurrences for eight subsamples. These data were also arcsin-transformed as outlined above to approximate normal distributions prior to the calculation of the mean values ((1 SD) shown. Radiochemical Analysis. For Po-210 and Pb-210 analyses, yield tracers (Po-208 and stable Pb) and Bi carrier were added to the dry subsamples, followed by wet-digestion using nitric acid and peroxide, with a final perchloric acid digestion to remove residual organics. After Fe removal from a 6 M HCl solution using ether, an extraction using 1% DDTC in chloroform was performed on the HCl solution, following dilution to 1.5 M to remove Po, Bi, and Pb. The dried DDTC extract was then dissolved in xylene from which the Pb and Bi were back-extracted, first with 7 M HCl, and then Po was recovered using 8 M HNO3. For Pb-210 analyses, a Pb(Bi)CrO4 precipitate was captured on a 0.22-mm membrane filter
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that was dried and then mounted on a stainless steel planchette using an adhesive tape that also acted as a weak β- and R-blocker. The planchette was then placed into a Canberra 2404 gas-flow proportional counter for 100 min to detect Bi-210 in equilibrium with Pb-210. Detection efficiency was determined using reference samples run in sequence with unknowns. Following counting, the membrane was dissolved, and the chemical yield was determined by stable Pb analyses using AAS. Po-210 was autodeposited on polished silver disks from a 0.1 M HCl solution at 75 °C and pH 1.5. Hydroxylamine was added as a reducing agent. The disks were then counted for up to 7000 min or until sufficient counts had been detected, with a surface barrier R-spectrometer. Calculated ingrowth from Pb-210 was then subtracted from the Po-210 values obtained, which were then corrected back to the date of collection. Analytical Quality Assurance. Three laboratories (ANSTO, Australia; Service Central de Protection Contre les Rayonnements Ionisants (SCPRI), France; and Laboratoire d’Etude et de Surveillance de l’Environnement (LESE), French Polynesia) were involved in an intercomparison exercise of Po-210 measurements in zooplankton subsamples. Because not all replicated subsamples were analyzed by all three laboratories, the intercomparison was based on (a) a subset of eight sample analyses by the three laboratories and (b) 14 samples that had been analyzed by both LESE and ANSTO. For comparison (a), a single factor analysis of variance was performed, which showed a significant difference (F ) 13.78, P < 0.001, n ) 24) between laboratories. For comparison (b), the results again showed a significant difference (t ) 4.83, P < 0.001, n ) 14) between ANSTO and LESE, with the LESE mean again being lower than that based on ANSTO analyses. Accordingly, Po210 determinations for samples analyzed by LESE were adjusted upwards by a factor of 1.27, which was the converse of the mean of the average of the two percentage differences with ANSTO results and the single percentage difference with SCPRI results.
FIGURE 1. Taxonomic composition of zooplankton from French Polynesian waters. Less abundant taxonomic groups that are not shown include, in descending order of abundance: lamellibranch larvae, mysids, siphonopterans, euphausiids, cnidarian medusae, isopods, doliolids, pisces larvae, decapoda, heteropoda, and gastropod larvae.
Results and Discussion Zooplankton were predominantly Copepoda (mean ) 70%, mostly Calanoids) (Figure 1) (13), being similar in taxonomic composition to zooplankton collections taken in the vicinity of Mururoa and Fangataufa Atolls (14). The frequency distribution of their mean lengths (arcsin-transformed) is shown in Figure 2; approximately 60% fell within 0.5-0.95 mm in length, and 80% fell between 0.5 and 1.95 mm. For this subset (Table 1), which had also been characterized as to taxonomic composition (Figure 1), a multiple linear regression of their Po-210 concentration against arcsintransformed (i) proportional abundance of Copepoda and (ii) proportional abundance of zooplankton of length range 0.5-0.95 mm showed neither were significant (F ) 1.61; P ) 0.39; n ) 8) predictors. Po-210 concentrations were determined in 27 zooplankton samples, including an interlaboratory comparison (ANSTO, Australia; SCPRI, France; and LESE, French Polynesia) that showed only minor (ca. 25%; P < 0.05) analytical differences between laboratories for replicates as compared to betweensample variation. In fact, these Po-210 concentrations in zooplankton, shown as a frequency distribution in Figure 3A, ranged over a factor of 60 from ca. 50 to 3200 Bq/kg (dry weight), with a median value of 1000. In Figure 3B is shown a frequency distribution of published values (15-20) for Po210 in marine zooplankton from a broad range of geographical locations giving a median value of about 200 and a much reduced upper limit as compared to the levels we have found in French Polynesian samples. This comparison highlights the degree of enhancement of Po-210 in the French Polynesian zooplankton samples, despite the remoteness of the region from continental sources of Po-210’s progenitor, Rn-222.
FIGURE 2. Length frequency distributions of zooplankton. Variation in taxonomic composition and size frequency distribution, factors reported to influence Po-210 concentration in zooplankton (15, 21), did not significantly (P > 0.05) affect Po-210 concentration within an albeit small set of data available to us (Table 1). However, Po-210 concentration shows an inverse and profoundly nonlinear relationship with zooplankton biomass (Figure 4). As zooplankton density
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TABLE 1. Showing Po-210 Concentration, Size, and Taxonomic Characteristics for Zooplankton Samples from French Polynesia
no.
Po-210 concn (Bq/g DW)
proportional abundance of Copepoda (arcsin-transformed)
proportional abundance of zooplankton within 0.5-0.95 mm length range (arcsin-transformed)
1 2 3 4 5 6 7 8
607 433 528 212 186 102 65 51
60.4 56.7 66.6 61.4 63.4 54.3 38.9 58.3
53.1 50.5 38.3 49.7 60.3 52.2 54.6 48.8
FIGURE 3. Frequency distribution of Po-210 concentrations in marine zooplankton from (A) French Polynesia and (B) various geographical locations, as reported in refs 15-20 (n ) 66). declines from 5.44 to 1 mg (dry weight)/m3, the Po-210 concentration remains approximately constant [mean ) 640 Bq/kg (dry weight); n ) 13]; reduction from 1 to 0.14 mg (dry weight)/m3 corresponds with an exponential increase in Po210 concentration to 3200 Bq/kg (dry weight). To interpret Figure 4 solely as a physiologically-based allometric relationship, as demonstrated within various taxa
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FIGURE 4. Polonium-210 concentrations in zooplankton samples from French Polynesian waters as a function of their biomass in water. The archipelagoes in closest proximity to the sampling sites were (b) Australs, (() Marquesas, (1) Society, and (2) Tuamotu/ Gambier. (21), would require individual zooplankton mass to decline systematically with reducing biomass from ca. 1 to 0.14 mg (dry weight)/m3, but not in such a way from 5.44 to about 1 mg (dry weight)/m3 where Po-210 concentrations are relatively constant. Such an explanation seems implausible. Moreover, for that subset of zooplankton samples, which were characterized for their size frequency distributions, there was no significant (P > 0.05) effect of biomass on the proportional abundance of individual zooplankters in the most abundant length category of 0.5-0.95 mm (Figure 2). Rather than seeking only a physiological interpretation of this relationship (Figure 4), we employ below a broader biogeochemical framework, incorporating the ability of zooplankton (mainly Copepoda) to both reduce the Po-210 water concentration by its removal from the euphotic zone (3, 5) and to reflect the resulting water concentration in their elevated tissue levels (22). In a simple a priori mathematical model, we propose that the mechanistic relationship between the steady-state Po210 concentration in zooplankton (Cz) and their density in the euphotic zone is described by the following equations: (i) Cw ) R/k(1 - e-kt), an equation form with first-order loss kinetics commonly used in radioecological compartmental analysis (23) (ii) Cz ) Cw‚CF, where Cz is the Po-210 concentration in zooplankton (steady state); Cw is the Po-210 concentration in water (dissolved); CF is the concentration factor for Po-210 in zooplankton, which is the IAEA-recommended value of 30 000 wet weight (22); R is the rate of Po-210 input to the water column, predominantly from the entry of Pb-210 to the sea surface by wet and dry deposition and its in situ decay to Po-210; t is time; and k is the rate constant for loss of Po-210 from the euphotic zone of the water column, which is positively related to zooplankton density. The rate of removal of Po-210 from the euphotic zone is also greater than that for Pb-210 due to Po-210’s greater particle reactivity (10, 24). Therefore, each measured Po-210 concentration in zooplankton represents a steady-state between (a) the rate of Po-210 input to the euphotic zone, and its subsequent incorporation into zooplankton via its ingestion in association with phytoplankton and seston (4), and (b) the rate of Po-210 removal from the euphotic zone where zooplankton density determines the rate of production of faecal pellets, which in turn predominantly determine Po210 removal (3, 5). To test the validity of this model, we have fitted suitable parameter values, taken from the literature, to derive a relationship between Po-210 concentration in zooplankton as a function of zooplankton biomass. The chosen parameter values are described below.
FIGURE 5. Modeled relationships between zooplankton biomass and Po-210 concentration in zooplankton, based on variable input rates (R; Bq‚m-2‚year-1) of Po-210 to the water column, combined with variable fecal pellet production rates by zooplankton, that determine zooplankton biomass-dependent rates of loss of Po-210 from the water column (k; Bq‚mg of dry Copepod-1‚year-1). (b) R ) 25, k ) 0.017; (0) R ) 52, k ) 0.017; (9) R ) 25, k ) 0.0498; (2) R ) 52, k ) 0.0498; ()) R ) 25, k ) 0.083; (1) R ) 52, k ) 0.083. For the rate of Pb-210 input to the water column (R), the following empirical values were considered: (i) 80 Bq‚m-2‚year-1 for Fiji, (ii) 52 Bq‚m-2‚year-1 for Rarotonga (both values from ref 25), and (c) 25 Bq‚m-2‚year-1 for Enewetak (26). French Polynesia lies at a greater distance from continental landmasses than these three locations, with an expected corresponding reduced rate of Pb-210 input; therefore, we have chosen the lower two of these three values. This represents the annual input rate of Pb-210 to a 1 m2 column of water in the euphotic zone, extending to 200 m in these clear oceanic waters (27). Po-210 input would therefore be nearly equivalent to Pb-210 , with a delay period of about 3 half-lives (415 days) as Po-210 grows in from Pb210. In our model, the rate of removal of Po-210 from the water column depends on (a) the rate of fecal pellet production per unit mass of zooplankton and (b) Po-210 concentration in zooplankton fecal pellets. From the literature, it is clear that defecation rates in zooplankton are dependent on both their size and food type. For simplicity in this modeling exercise, we have chosen values of 0.05, 0.15, and 0.25 g of dry Copepod feces‚g of dry Copepod-1‚day-1, which is a range that lies within that found in the literature (28-30). For Po-210 in fecal pellets, we have used a value of 0.91 Bq‚g dry -1 reported for euphausiids (5). From these values, we derive the following rates of Po-210 removal by zooplankton faecal pellets; 0.017, 0.0498, and 0.0831 Bq‚g dry zooplankton-1‚year -1, at the three respective rates of fecal pellet production. To then convert model-predicted Po-210 water concentration to Po-210 concentration in zooplankton, we have used the IAEArecommended concentration factor of 3 × 104 (22), with a wet weight:dry weight conversion factor for zooplankton of 7.5 that was previously measured in French Polynesian samples (6). In Figure 5 are shown the resulting modeled relationships between zooplankton biomass and Po-210 concentration in zooplankton, based on the six combinations of empirical k and R values given above. The shape of these relationships is clearly comparable to that found in French Polynesian zooplankton (Figure 4). Also, the ranges of Po-210 concentrations predicted by the model at each zooplankton biomass encompass the levels measured in French Polynesian zooplankton. So, although the parameter values used in this modeling exercise are not specific to French Polynesia, these results indicate the model’s capacity to simulate the empirical relationship between zooplankton biomass and Po-210 concentration in zooplankton (Figure 4).
FIGURE 6. Relationship between absolute Po-210 water concentration (dissolved) and the ratio of Pb-210: Po-210 water concentrations (dissolved) in surface waters of the Pacific; (9) inclusive of the region of zooplankton sampling, (b) exclusive of the region of sampling. Data taken from ref 9. Our empirical results and mathematical model, which fits the relationship (Figure 4), are also consistent with the following established characteristics of the euphotic zones in oligotrophic marine environments as compared to contiguous regions of higher productivity: (i) Enhanced mean residence times of Pb-210 (31). (ii) Enhanced Pb-210 concentrations in zooplankton from Atlantic gyres and the Caribbean and a reduced ratio of Pb210:Po-210 concentrations in zooplankton (10). (iii) Reduced ratios of the water concentrations (dissolved) of Pb-210:Po-210 in the Eastern Pacific gyre, which included measurements in the geographical region from which zooplankton were collected for this study (9). Our proposal for the existence an inverse relationship between absolute Po-210 water concentration and biological productivity, which underpins the relationship show in Figure 4, is also supported by observed decreased inventories of Pb-210 and Po-210 in surface waters of Funka Bay, Japan, that was attributed by the authors to a phytoplankton bloom and associated increased production of particulate matter (24). Most significant for the critical support of our mechanistic model is the following derivation. From GEOSECS data (9) for Pb-210 and Po-210 concentrations (dissolved) in the surface waters of the Pacific, inclusive of the region from which zooplankton in our study were taken, we have derived the relationship (Figure 6) between absolute Po-210 water concentration and the ratio of Pb-210:Po-210 concentrations in water that is considered to be a relative measure of biological productivity (10, 11). This inverse relationship is very similar in shape to both our empirical and theoretical curves (Figures 4 and 5), and the following log-log regression equations confirms its statistical significance. For waters sampled within the region from which zooplankton were sampled for this study: Po-210 water concentration (log10) ) -0.91-1.03[(Pb-210: Po-210 water concentrations) log10]; r2 ) 0.88, P < 0.0001, n ) 11. For the larger number of samples of waters taken outside of this region: Po-210 water concentration (log10) ) -1.00-0.51[(Pb-210: Po-210 water concentrations) log10]; r2 ) 0.19, P ) 0.0045, n ) 42. These results represent very strong support for our hypothesized model (see above). Because of the commonality of zooplankton-mediated removal of radionuclides from the euphotic zone (1, 2), it follows that the above model for Po210 would operate for other particle-reactive nuclides. For potential future leakage of such nuclides into the oligotrophic oceanic environments close to the former weapons tests sites
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at Mururoa and Fangataufa and recently proposed radioactive waste repositories at the Marshall Islands and Palmyra Atoll (8, 32, 33), the generally low densities of zooplankton may, in effect, enhance the concentrations of these anthropogenic radionuclides in the surrounding waters. Consequently, enhanced levels could be expected in zooplankton themselves, in accordance with their established concentration factors (22). For that subset of nuclides that are also assimilated via food intake like Po-210 (34, 35), e.g., Cs-137, Co-60, and Zn65, enhanced concentrations might occur at higher trophic levels. This interpretation is also consistent with the recent finding of elevated Po-210 concentrations in fish from the oligotrophic waters of the Marshall Islands relative to levels found in fish from higher productivity waters of Northern Europe (36).
Acknowledgments We thank those that took part in the collection and analysis of samples, including staff from SCPRI, France; ANSTO, Australia, and LESE, Tahiti, particularly Mr. C. Poletiko. The results used in this investigation were a component of a broader Australia/France bilateral research program on the use of zooplankton to monitor radionuclides in the Pacific Ocean. Comments from Y. Nozaki, N. Fisher, and an anonymous reviewer greatly improved the manuscript. The IAEA Marine Environment Laboratory operates under a bipartite agreement between the International Atomic Energy Agency and the Government of the Principality of Monaco.
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(10) Turekian, K. K.; Kharkar, D. P.; Thomson, J. Earth Planet. Sci. Lett. 1974, 32, 304-312. (11) Kadko, D. J. Geophys. Res. 1993, 98 (C1), 857-864. (12) Newell, G. E.; Newell, R. C. Marine Plankton: A Practical Guide; Hutchinson & Co.: London, 1977. (13) Zar, J. H. Biostatistical Analysis; Prentice Hall: Englewood Cliffs, NJ, 1996. (14) Ballestra, S.; Noshkin, V. IAEA-ILMR Report 48; 1991, pp 12. (15) Swarzek, B.; Bojanowski, R. Mar. Biol. 1988, 97, 301-307. (16) Cherry, M. I.; Cherry, R. D.; Heyraud, M. Mar. Biol. 1987, 96, 441-449. (17) Heyraud, M.; Cherry, R. D. Mar. Biol. 1979, 52, 227-236. (18) Heyraud, M.; Domanski, P.; Cherry, R. D.; Fasham, M. J. R. Mar. Biol. 1988, 97, 507-519. (19) Carvalho, F. P. Radiat. Prot. Dosim. 1988, 24 (1/4), 113-117. (20) Shannon, L. V.; Cherry, R. D.; Orren, M. J. Geochim.Cosmochim. Acta 1970, 34, 701-711. (21) Cherry, R. D.; Heyraud, M. In Radionuclides in the Study of Marine Processes; Kershaw, P. J., Woodhead, D.S., Eds.; Elsevier Applied Science: London and New York, 1991; pp 309-318. (22) IAEA. Tech. Rep. Ser. 247, 1985. (23) Whicker, F. W.; Schultz, V. Radioecology: Nuclear energy and the environment; CRC Press: Cleveland, 1982; Vol. 2. (24) Tanaka, N.; Takeda, Y.; Tsunogaii, S. Geochim. Cosmochim. Acta 1983, 47, 1783-1790. (25) Turekian, K. K.; Nozaki, Y.; Benninger, L. K. Annu. Rev. Earth Planet. Sci. 1977, 5, 227-255. (26) Turekian, K. K.; Cochran, J. K. Nature 1981, 292, 522-524. (27) Clark, G. L.; Denton, E. J. Light and Animal Life. In The Sea, Ideas and Observations on Progress in the Study of the Seas; Hill, M. M., Ed.; Interscience: New York, 1962; pp 456-468. (28) Small, L. F.; Fowler, S. W.; Moore, S. A.; La Rosa, J. Deep-Sea Res. 1983, 30, 1199-1220. (29) Small, L. F.; Ellis, S. G. Prog. Oceanog. 1992, 30, 197-221. (30) Miquel, J. C.; Fowler, S. W. unpublished data. (31) Schell, W. R. Geochim. Cosmochim. Acta 1977, 41, 1019-1031. (32) The Australian, Sept. 26, 1996, p 13. (33) Herald Sun (Melbourne), 1st ed., May 31, 1996, p 29. (34) Carvalho, F. P. Health Phys. 1995, 69, 469-480. (35) Carvalho, F. P.; Fowler, S. W. Mar Ecol. Prog Ser. 1994, 103, 251-264. (36) Noshkin, V. E.; Robison, W. L.; Wong K. M. Science Total Environ. 1994, 155, 87-104.
Received for review December 20, 1996. Revised manuscript received April 15, 1997. Accepted May 2, 1997.X ES9610592 X
Abstract published in Advance ACS Abstracts, July 1, 1997.
