Allometric relationships for radioecological parameters in marine biota

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1 Allometric relationships for radioecological parameters in marine biota Vives i Batlle, J. 1,a, Wilson, R.C. a, Watts, S.J. a, McDonald, P. a and Craze, A. b a Westlakes Scientific Consulting Ltd., The Princess Royal Building, Westlakes Science and Technology Park, Moor Row, Cumbria, CA24 3LN, UK. b Nuclear Decommissioning Authority, Herdus House, Westlakes Science and Technology Park, Moor Row, Cumbria, CA24 3HU, UK INTRODUCTION Exchange rate and bioaccumulation of radionuclides in biota are commonly represented by two simple parameters: the biological half-life of elimination (T B1/2 ) and the concentration factor (CF), which is the activity concentration of a radionuclide in the organism relative to the medium. Reliable CF and T B1/2 data are limited to common marine organisms and radionuclides. The present study addresses this problem by presenting an interpolation method based on allometric scaling of radionuclides for plankton, seaweed, fish, crustaceans and molluscs. b Power relationships of the type Y = a M (where Y represents the CF or the long term component of the TB1/2) were fitted to a biokinetic database. It was expected that b would be close to the slope of ¼ frequently found in allometric relationships in biology (Cherry and Heyraud, 1991). It was also expected that a would depend on the individual properties of compounds formed by radionuclides in the marine environment. Previous work by us (Vives i Batlle et al., 2007) had already found allometric formulae for the CF of Pu and Am and T B1/2 of Cs and Tc. These appeared consistent with previous studies, suggesting that for the CF b is about ¼ and for the T B1/2 it varies between +0.1 and +0.3 (Table 1). MATERIALS AND METHODS The dataset of biokinetic parameters for Tc, I, Cs, Pu and Am in fish, crustaceans, molluscs, plants and plankton reported in Vives i Batlle et al. (2007; 2008) was used in this study. To this was added data for 29 additional elements. For the T B1/2 this includes Cm data from Swift (1995) and Po from Swift et al. (1995) (winkles), Ag, Co, Eu, Mn and Zn from Boisson et al. (1997) and Mn and Co data from Carlson (1994) (macrophytes), C data from Fievet et al. (2006) (macrophytes and molluscs) and Se data from Alquezar et al (2007; 2008) (fish, crustaceans and molluscs). The CF database was expanded using data from IAEA (2004). Table 1. Allometric relationships for CF and T B1/2 from previous work Parameter log 10 [CF(m 3 kg -1 )] log 10 [T B1/2 (d)] Pu a,b Am a,b Po c Pb c Cs a,b Cs d Sr d I d Tc a,b Log 10 a n/a n/a b r n/a n/a 0.92 n/a n/a n/a 0.74 p n/a n/a 0.04 n/a n/a n/a 0.03 N n/a n/a 4 n/a n/a n/a 6 Notes: a Converted from y = a V b with V in m 3 to = a M b with M in kg using a density of 10 3 kg m -3. References: b Vives i Batlle et al. (2007). c Cherry and Heyraud (1991). d Eqs. 15a - 19 from Higley et al. (2003) 2 1 * Corresponding author. Fax: +44 (0) address: jordi.vives@westlakes.ac.uk 2 From USDOE (2002) Section , in turn quoting Whicker and Schultz (1982) and ultimately Kitchings et al. (1976). Only the original source gives the units for the T B1/2 in days, as shown here.

2 For both CFs and T B1/2 we calculated, using bespoke statistical software, the parameters a and b b for Y = a M. We also calculated the coefficient of determination, r 2 and the p-value of the two-tailed Student T-test. To discriminate potentially significant relationships, we used the triple criteria that r 2 > 0.7, p < 0.05 and N > 2. RESULTS Of the 34 independent regressions calculated for the CF, there were 8 for which allometric relationships satisfying the triple criteria were found (Table 2). What these elements have in common (with the exception of Ra and Ru) is being lanthanides or actinides. The fitted parameters are consistent with previous work (Vives i Batlle et al., 2007). Additionally, five other regressions (Mn, Zr, Po, Ac and Pa) showed slopes significantly different from ¼ (Ttest p < 0.05), although r 2 is only between 0.4 and 0.6 in these cases. Therefore, for the data showing strong correlations, a mean slope of 0.26 ± 0.09 is supported, a confirmation of allometric scaling to a quartile power of the mass for marine biota, as predicted theoretically 3. Table 2. Allometric relationships for CF and T B1/2 from the present work Parameter log 10 [CF(m 3 kg -1 )] log 10 [T B1/2 (d)] Ru Ce Pm / Eu Ra Th Pu Am Cm Tc Cs Pu Am Log 10 a b r SE Loga SE b p N The intercept log 10 (a) ranges from 1.5 to +0.2, which implies a two order of magnitude range of variation in a. This important variability is thought to relate to the physico-chemical speciation of different radioelements in seawater. In an attempt to verify this hypothesis we plotted log 10 (a) as a function of various parameters including atomic mass, electronegativity, ionic radius and oxidation state, with negative results. Noticing a general tendency for the more sediment-seeking nuclides to register the highest values, we uncovered a statistically significant trend with the logarithm of the sediment-water partition coefficient, or K d (Figure 1). This trend improves greatly with the removal of Ru, Eu and Pm (log 10 (a) = 0.22 log 10 (K d ) - 1.1, r 2 = 0.88, p = 0.006, N = 6). An association between the CF and the K d was previously suggested by Copplestone et al. (2003), who noted this relationship works only for radionuclides in a cationic form. Our work confirms this, as the majority of radionuclides correlating with K d are cations and the few nuclides likely to be present as anions (such as Ru) tend to be outliers in Figure 1. In addition to the two T B1/2 relationships for Tc and Cs identified by Vives i Batlle et al. (2007), the current study has uncovered a statistically significant formula for Am and a potentially significant one for Pu 4 (Table 2). Taken together, these three relationships support an intercept of ± The intercept ranges from 1.73 for Cs and 1.99 for Tc (more 3 Tritium is a special exception, as CFs for this radionuclide are defined as being 10-3 m 3 kg -1 for all organisms. 4 In the latter case, N = 3 and with such few data a p-value of 0.2 is generated, though r 2 = 0.9 and the allometric parameters are consistent with those found for Am.

3 predominantly conservative radionuclides) to 2.40 for Am and 2.80 for Pu (both particleseeking, non-conservative nuclides). 0.4 Log(a, m^3 / kg) ,155 Eu, 147 Pm Log 10 (a) = 0.34 x Log 10 (K d ) R 2 = 0.57, P = Ru Log(Kd, m^3 / kg) Figure 1. Trend between the allometric parameter a and the K d The standard errors for the intercept and slope given in Table 2 (SE loga and SE b ) can be used to perform uncertainty estimations in the CF and T B1/2 when allometric equations are used in predictive mode. For this it is only necessary to use the simple maximising error propagation y formula = log 10 ( a) + b log 10 ( M ). For most species the absolute value of y ln(10) log(m) ranges between 1 to 2 except for phytoplankton (10) and zooplankton (4). According to this, on the basis of statistical uncertainties, CF and T B1/2 predictions would range from % for macroscopic animals and plants and % for plankton. In practice, the allometric formulae reproduce the CF quite well, with 70% of the values within a factor of 2 or less difference and only 8% of the values a factor of 5 or more. For the T B1/2 the percentage is 90%, with no values in excess of a factor of 4. DISCUSSION AND CONCLUSIONS A consistent picture seems to emerge from our results. The elements that scale allometrically with a quartile power of the mass in marine biota are mostly lanthanides and actinides. Association of a with the K d suggests the former being highest for particle-seeking elements, most likely binding to biological / organic matter. We hypothesise that, for the elements that correlate allometrically, the driving uptake process may be ingestion rather than passive uptake from water, which is surface area rather than mass-dependent. Metabolic theory predicts that the whole body metabolism scales to M ¾ (McMahon, 1973; West et al., 1997). This is what drives the ingestion rate scaling to M ¾ predicted for land animals (USDoE, 2002). The observed scaling of the CF to M -¼ is compatible with this, as the CF is the activity concentration (normalised against mass) in the organism relative to the medium. The observed scaling of T B1/2 to the power of +0.16, based on limited data, is compatible with the range to reported by USDoE(2002). If potential statistical consistency with +¼ at ± 3σ is further confirmed, this would be consistent with the prediction that turnover rate

4 constants (proportional to T B1/2-1 ) generally decrease with mass at an exponent of ¼ (Hendriks, 2007). In conclusion, the work presented here provides a method to address data gaps in transfer for marine biota, based on allometry. Our findings are related at a fundamental level to metabolism. As a first test of application this method is being implemented in the dynamic model for the assessment of radiological exposure to marine biota developed by these authors (Watts et al., 2008), resulting in a wider range of applicability for this model. References Alquezar, R., Twining, J.R., Markich, S.J. (2007). Uptake and loss of 109 Cd and 75 Se in estuarine macroinvertebrates. Chemosphere 67: Alquezar, R., Markich, S.J., Twining, J.R. (2008). Comparative accumulation of 109 Cd and 75 Se from water and food by an estuarine fish (Tetractenos glaber). J. Environ. Radioactiv. 99: Boisson, F., Hutchins, D.A., Fowler, S.W., Fisher, N.S., Teyssie, J-L. (1997). Influence of temperature on the accumulation and retention of 11 radionuclides by the marine alga Fucus vesiculosus (L.). Mar. Pollut. Bull. 35(7-12): Carlson, L. (1994). Uptake and release of 54 Mn and 60 Co in Fucus vesiculosus L. and its epiphytes. J. Environ. Radioact. 22(1): Pages Cherry, R.D., Heyraud, M. (1991). Polonium-210 and lead-210 in marine organisms: allometric relationships and their significance. In: Radionuclides in the Study of Marine Processes. PJ Kershaw, DS Woodhead, editors. Elsevier Applied Science, London and New York, pp Copplestone, D., Wood M., Bielby S., Jones S.R., Vives J., Beresford N.A. (2003). Habitats regulations for Stage 3 assessments: radioactive substances authorisations. Environment Agency R&D Technical Report P3-101/SP1A, October 2003, 104 pp. Fiévet, B., Voiseux, C., Rozet, M., Masson, M., Bailly du Bois, P. (2006). Transfer of radiocarbon liquid releases from the AREVA La Hague spent fuel reprocessing plant in the English Channel. J. Environ. Radioactiv. 90(3): Hendriks, A.J. (2007). The power of size: A meta-analysis reveals consistency of allometric regressions. Ecol. Modelling 205(1-2): Higley, K.A., Domotor, S.L., Antonio, E.J. (2003). A kinetic-allometric approach to predicting tissue radionuclide concentrations for biota, J. Environ. Radioactiv. 66: International Atomic Energy Agency (2004). Sediment Distribution Coefficients and Concentration Factors for Biota in the Marine Environment. Technical Reports Series No. 422, Vienna. IAEA STI/DOC/010/422. Kitchings, T., DiGregorio, D., Van Voris, P. (1976). A review of the ecological parameters of radionuclide turnover in vertebrate food chains. In: Cushing, C.E. (Ed.), Radioecology and Energy Resources. Dowden, Hutchinson & Ross, Stroudsburg, PA, pp McMahon, T.A. (1973). Size and shape in biology. Science 179: Swift, D.J. (1995). A laboratory study of 239,240 Pu, 241 Am and 243,244 Cm depuration by edible winkles (Littorina littorea L.) from the Cumbrian Coast (NE Irish Sea) radiolabelled by Sellafield discharges. J. Environ. Radioactiv. 27: Swift, D.J., Smith, D.L., Allington, D.J., Winpenny, K. (1995). A laboratory and field study of 210 Po depuration by edible winkles (Littorina littorea L.) from the Cumbrian Coast (north-eastern Irish Sea). J. Environ. Radioactiv. 26 (2): USDoE (U.S. Department of Energy) (2002). DOE Standard: A Graded Approach for Evaluating Radiation Doses to Aquatic and Terrestrial Biota. Module 3: Methods Derivation. DOE-STD , Washington DC, 58 pp. Vives i Batlle, J., Wilson, R.C., McDonald, P. (2007). Allometric methodology for the calculation of biokinetic parameters for marine biota. Sci. Total. Environ. 388 (1-3):

5 Vives i Batlle, J., Wilson, R.C., Watts, S.J., Jones, S.R., McDonald, P., Vives-Lynch, S (2008). Dynamic model for the assessment of radiological exposure to marine biota. J. Environ. Radioactiv. doi: /j.jenvrad Watts, S.J., Vives i Batlle, J., Wilson, R.C., Jones, S.R., McDonald, P. Dynamic modelling for the assessment of radiation impacts on biota and man using Excel VBA and related extensions of the ERICA assessment methodology. In: Proc. International conference on radioecology and environmental radioactivity, June 2008, Bergen, Norway. West, G.B., Brown, J.H., Enquist, B.J. (1997). A general model for the origin of allometric scaling laws in biology. Science 276: Whicker, F.W, Schultz, V. (1982). Radioecology: Nuclear Energy and the Environment. Vols. I and II. Boca Raton, Florida: CRC Press.

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