Transuranic biokinetic parameters for marine invertebrates—a review

Environment International 28 (2002) 83 – 96 www.elsevier.com/locate/envint

Transuranic biokinetic parameters for marine invertebrates—a review T.P. Ryan* Radiological Protection Institute of Ireland, 3 Clonskeagh Square, Clonskeagh Road, Dublin 14, Ireland Received 30 September 1999; accepted 7 February 2002

Abstract A catalogue of biokinetic parameters for the transuranic elements plutonium, americium, curium, neptunium, and californium in marine invertebrates is presented. The parameters considered are: the seawater – animal concentration factor (CF); the sediment – animal concentration ratio (CR); transuranic assimilation efficiency; transuranic tissue distribution and transuranic elimination rates. With respect to the seawater – animal CF, authors differ considerably on how they define this parameter and a seven-point reporting system is suggested. Transuranic uptake from sediment by animals is characterised by low CRs. The assimilation efficiencies of transuranic elements in marine invertebrates are high compared to vertebrates and mammals in general and the distribution of transuranics within the body tissue of an animal is dependent on the uptake path. The elimination of transuranics from most species examined conformed to a standard biphasic exponential model though some examples with three elimination phases were identified. D 2002 Elsevier Science Ltd. All rights reserved. Keywords: Invertebrate; Concentration factor; Transuranic

1. Introduction Transuranic elements are mainly present in the marine environment as a result of atmospheric nuclear weapons tests, discharges from commercial nuclear activities, local accidents, and accidents involving both radioisotope-powered satellites and nuclear weapons. Some of the isotopes of these elements will persist in the environment for tens of thousands of years because of the length of their radioactive half-lives. Transuranic radionuclides such as plutonium(IV) and americium(III) are strongly particulate reactive and on entering the marine environment can be transported to the bottom sediments. Marine invertebrates, particularly sediment-dwelling species, can play a role in the recycling of transuranic nuclides released into the marine environment. They can act to redistribute radionuclides deposited in the sediments of the sea floor by agitating and mixing the sediment as they burrow, feed, and excrete. The marine invertebrates are contaminated by ingesting contaminated sediment, seawater, and food. This contamination can be passed on to predatory animals or, indeed, to humans, and in this way the radionuclides can

* Tel.: +353-1-269-7766; fax: +353-1-269-7437. E-mail address: [email protected] (T.P. Ryan).

find a route into the food chain. This review brings together data which may be useful in the development of biokinetic models for transuranic nuclides which take account of the invertebrate vector.

2. Biokinetic parameters 2.1. Seawater –animal concentration factors (CFs) The relationship between radionuclides, such as the transuranic elements in the marine environment, and marine invertebrates, is generally described by the use of CFs although alternative mechanistic-based kinetic models have been suggested (LeFur et al., 1991). This review focuses on the more common approach. The seawater – animal CF is generally defined as the ratio between the activity concentration of the radionuclide in the animal (wet weight) and the activity concentration of the radionuclide in the ambient seawater (Eq. (1)). Sometimes the activity concentration in the seawater is defined in terms of becquerel per milliliter (Bq ml
1) as opposed to becquerel per gram (Bq g
1), which results in admittedly small differences due to the density of seawater. Expressing the activity in water in terms of becquerel per gram has an advantage in that the resulting CF coefficient is without units.

0160-4120/02/$ – see front matter D 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 1 6 0 - 4 1 2 0 ( 0 2 ) 0 0 0 11 - 9

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T.P. Ryan / Environment International 28 (2002) 83–96

In theory, it is possible to estimate the activity concentration of the radionuclide in animals exposed to the contaminated seawater given knowledge of the relevant CFs and the activity concentration of the radionuclide in the seawater. CFs can be used subsequently to plot the path of the radionuclide from seawater into the food chain. Shulte (1997) provides a useful mathematical treatment of CFs. This makes knowledge of CFs for radionuclides and marine animals potentially valuable in producing models, particularly in a radiological protection context. Seawater
Animal CF ¼

Activity Concentration of Animal ½Bq g
1 ; wet weight Activity Concentration of Ambient Water ½Bq g
1 

(1)

The volume of data on seawater – animal CFs for transuranic elements in marine invertebrates in the literature is not overwhelming. A cautious approach to data interpretation should be taken as differences in experimental procedures such as filtration methodologies, animal exposure time, biological parameters, and physical and chemical speciation are considerable. While CFs for a range of animals are reported, there is very little duplication in the literature making data comparison and confirmation difficult. The most widely reported CFs are for plutonium and, to a lesser extent, for americium and curium with few data for neptunium and californium. CFs were estimated in the course of the following studies mentioned below. Noshkin (1972) reviewed the ecological aspects of plutonium behavior in aquatic systems with a focus on uptake from sediments and seawater. Fowler and Heyraud (1974) examined the retention of americium by plankton. Fowler et al. (1975) performed laboratory experiments to examine plutonium uptake by invertebrates and the effect of moulting and the presence of byssus treads on plutonium body burdens. Bowen et al. (1976) examined the bioavailability of plutonium to biota of the north Atlantic where measurements were in situ rather than laboratory based. Guary and Fowler (1977) examined the biokinetics of neptunium in mussels and shrimp. They identified surface absorption as important in the uptake process and moulting as important in the loss stage. Guary and Fraizier (1977) examined the relationship between plutonium uptake and trophic level and they observed a relationship between the rate of uptake and the calcified structures of certain marine species. Guary and Fowler (1978) examined the uptake of neptunium from seawater by crabs, shrimp, and mussels. They noted that the highest CFs were for the shells of the animals and concluded that the behavior of neptunium in the animals was very similar to that of plutonium. IAEA (1978) provides a list of recommended ranges of CFs for a comprehensive set of nuclides including plutonium, americium, curium, neptunium, and californium. Murray et al. (1978) studied the accumulation of americium in invertebrates found in both the marine environment and those dwelling

in brackish waters. Kurabayashi et al. (1979) determined CFs in a range of crustaceans and molluscs for use in environmental dose assessment projects. Grillo et al. (1981) examined the uptake characteristics of plutonium, americium, and curium by a range of molluscs, echinoderms, and annelids in a laboratory study. They found that in general the order for accumulating transuranics in their studies was annelids followed by molluscs and then echinoderms. They found that with one notable exception (a brittle star), the uptake of americium over plutonium was substantial in the species examined and they observed similar behavior between americium and curium. Guary et al. (1982) investigated plutonium uptake by starfish and found that while plutonium in seawater has a strong affinity for the mucusrich epidermal layer, biomagnification does not occur. Guary and Fowler (1982) studied the behavior of plutonium and americium in the cephalopod Octopus vulgaris after exposure to labelled seawater where they observed a more rapid accumulation of plutonium over americium. Miramand et al. (1982), though primarily concerned with the uptake of americium and plutonium from sediments, reported data for CFs for the benthic species Arenicola marina, Corophium volutator, and Scrobicularia plana. Carvalho and Fowler (1984) examined the uptake of americium from seawater by a range of invertebrates. They noted in particular the role of mucus produced by some polychaetes in enhancing accumulation of americium and concluded that whole body burdens of americium can fluctuate in accordance with mucus production. Pentreath (1984), in determining uptake of plutonium and americium by invertebrates from seawater, highlighted the difference in the magnitude of CFs when calculated on the basis of both filtered and total seawater. Carvalho and Fowler (1985a) studied the behavior of plutonium, americium, and californium in a marine isopod. They observed differences in uptake and turnover rates of different chemical species of plutonium in the isopods. Higher CFs were found for americium and californium than for plutonium. Fowler and Carvalho (1985), in an experiment designed to elucidate americium biokinetics in benthic organisms as a function of feeding mode, found that americium accumulation from seawater by echinoderms increases with the degree of calcification of the body wall. IAEA (1985a) provides a revised list of recommended ranges of CFs for a comprehensive set of nuclides including plutonium, americium, curium, neptunium, and californium. Fowler et al. (1986) performed laboratory experiments to assess californium bioavailability to marine invertebrates. They observed the prominent role of surface sorption in the uptake process from seawater, which was evidenced by the preponderance of californium present on the exoskeletons of exposed animals. Germain et al. (1987) designed experiments to look at the transfer of neptunium from seawater to annelids and molluscs. They found that the differences in CFs between the two species examined were due to the preferential uptake of neptunium on the shells of the molluscs.

T.P. Ryan / Environment International 28 (2002) 83–96

Miramand et al. (1987) confirmed in their observations the general similarity in uptake from seawater of americium and curium and the generally higher CFs that prevail for those nuclides over plutonium. Swift and Pentreath (1988) looked at the accumulation and turnover of plutonium in the edible winkle and observed that greater than 80% of the whole body activity was present on the shell after 50 days of exposure to labelled seawater. Germain and Pinte (1990) provide a discussion on the transfer modes of neptunium to various marine species as a function of their trophic level. Hayashi et al. (1990) measured in situ CFs for plutonium and americium in marine species including molluscs and crustaceans and noted in particular that the CF values for americium are generally higher than those for plutonium. Miramand et al. (1991) observed the uptake of americium from seawater by the scallop Pecten maximus and used histo-autoradiography to determine its distribution throughout the tissue of the animal. CFs for 12 arthropods, 21 molluscs, 6 echinoderms, 3 annelids, 3 urocordates, 1 cnidarion, and 1 sponge were found in the literature and these are presented in Table 1. Each CF is presented, where possible, with relevant experimental parameters such as whether or not the measurement was a field measurement or a laboratory experiment, what type of filtration was used, as well as the exposure time. These parameters are encoded and can be accessed using the key provided at the bottom of the table. A number of generalised CFs were reported in the literature and these are also presented in Table 1 under the respective animal classifications.

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of americium and plutonium in sediment and their uptake by three sediment-dwelling species. They demonstrated the transfer of americium to the animals from interstitial water. Similarly, Vangenechten et al. (1983) looked at the uptake of americium from labelled deep-sea sediments. Germain et al. (1984) examined the uptake of plutonium and americium by sediment-dwelling animals exposed to labelled sediment. They concluded that for the animals they studied, the CRs were very low, and that while the predominant transfer pathway was interstitial water, they did observe some direct transfer between sedimentary particles and two annilids. Fowler et al. (1986) assessed the bioavailability of californium to sediment-dwelling invertebrates. Again, they found that transfer was characterised by low CRs with evidence to suggest that the main pathway was from the interstitial water. Swift and Pentreath (1988) examined the accumulation of plutonium by the edible winkle Littorina littorea. Accumulation from silt was found to be low. Table 2 includes CRs for two arthropods, three molluscs, and three annelids. From the limited data available, it appears that for transuranic elements the exchange between sediment and sediment-dwelling animals is characterised by low CRs. Sediment
Animal CR ¼

Activity Concentration of Animal ½Bq g
1 ; wet weight (2) Activity Concentration of Sediment ½Bq g
1 ; wet weight

2.2. Sediment – animal concentration ratios (CRs)

2.3. Radionuclide assimilation efficiencies and tissue distribution

It is well established that transuranic nuclides such as plutonium(IV) and americium(III) entering the marine environment are rapidly transported to the sediment. Sediment-dwelling animals may absorb radionuclides from direct contact with sediment, from ingestion, and from interstitial waters. The sediment – animal CR, defined by Eq. (2), is a quotient that can be useful in the evaluation of the significance of the sediment – animal pathway in the transfer of radionuclides into the food chain. Some authors report CRs on a dry weight basis, but once the dry to wet weight ratios are quoted, comparison between different data sets is possible. There are few CRs for transuranics (plutonium, americium, and californium) and marine invertebrates available. CRs were calculated in the course of the following studies mentioned below. Beasley and Fowler (1976) compared the uptake of 238Pu and 239,240Pu by deposit-feeding marine worms living in sediments and concluded that no difference in uptake exists between the isotopes. However, Clifton et al. (1983), in their studies, were unable to discount observed discrimination between 238Pu and 239,240Pu and postulated differences in the initial speciation of the isotopes as a causative factor. Miramand et al. (1982) looked at the biological availability

When an animal ingests radioactive material such as the transuranic elements while feeding, the extent to which the radioactivity is initially taken up from the food by the animal is sometimes called the assimilation efficiency. It is expressed as a percentage of the total ingested activity. Studies have been carried out to examine the assimilation efficiencies of invertebrates for transuranic elements from labelled food in two-step food chain studies. The data are presented in Table 3. These systems involved feeding plutonium-labelled Artemia to the arthropod Lysmata seticaudata (Fowler et al., 1975); plutonium- and californiumlabelled Nereis diversicolor to the arthropod Carcinas maenas (Fowler and Guary, 1977; Guary and Fowler, 1982); americium-labelled Artemia to the arthropod Galathea strigosa (Fowler and Carvalho, 1985); americium- and californium-labelled fish muscle and mussel soft parts to the arthropod Cirolana borealis (Carvalho and Fowler, 1985a); americium-labelled Car. maenas to the mollusc O. vulgaris (Fowler et al., 1986); plutonium-labelled Fucus spiralis to the mollusc L. littorea (Swift and Pentreath 1988); and americium- and californium-labelled mussels to a selection of echinoderms (Fowler and Carvalho 1985; Fowler et al., 1986; Galey et al., 1983; Guary et al., 1982).

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Table 1 Transuranic sea water – animal CFsa Pu Phylum

Genus

Arthropoda

Gammarus locusta G. strigosa C. volutator Lys. seticaudata

Am

Cm

770 (21 days)[7] (LM, NFSW, UC) 665 (21 days)[7] (LM, NFSW, UC) 1050 (11 days)[11] (LM, FSW2, NE)

700 (11 days)[22] (LM, FSW2, NE)

750 (12 days)[11] (LM, FSW2, NE) 19 (25 days)[8] (LM, CFSW, NE)

Can. pagurus

Cf

15 – 20 (92 days)[25] (LM, CFSW, NE) 30 (50 days)[24] (LM, UC, E)

220 (21 days)[28] (LM, NFSW, E)

503[9] (FM, TSW) 1140 – 2520[14] (FM, UC) 1700 (48 days)[20] (LM, CFSW, UC) 125 (64 days)[20] (LM, CFSW, UC)

Artemia Meg. norvegica

665 (21 days)[28] (LM, NFSW, E)

Pilumnus hirtellus 171 – 436 [27] (FM, FSW2) 39 – 100[27] (FM, FSW2)

Car. maenas (carapace) Can. pagarus (carapace) Cir. borealis

General Crustacea (general)

Mollusca

Crustacea (general) V. decussata

Pu (III, IV) 52 (23 days)[19] (LM, NFSW, NE) Pu (V, VI) 54 (23 days)[19] (LM, NFSW, NE) (SP) 250[4] (FM, TSW) 100[16] (UC) 250[18] (FM) 300[12] (UC)

Cer. edule Scr. plana L. littorea

L. littoralis

190 (42 days)[11] (LM, FSW2, NE) 35 (50 days)[3] (LM, FSW2, E) (SP) 82 – 320 [13] (FM, TSW) (SP) 2.2k – 7.6k[13] (FM, FSW1) 205[9] (FM, TSW)

76 (23 days)[19] (LM, NFSW, NE)

185 (23 days)[19] (LM, NFSW, NE)

(SP) 550[4] (FM, TSW) 200[16] (UC)

200[16] (UC)

100[16] (UC)

200[16] (UC)

500[12] (UC)

500[12] (UC)

100[12] (UC)

500[12] (UC) 78 (21 days)[28] (LM, NFSW, E)

140 (28 days)[22] (LM, FSW2, NE) 230 (31 days)[11] (LM, FSW2, NE) (SP) 130 – 420[13] (FM, TSW) (SP) 22k – 43k[13] (FM, FSW1)

140 (28 days)[22] (LM, FSW2, NE) 80 (23 days)[22] (LM, FSW2, NE)

30 – 40 (13 days)[26] (LM, FSW2, NE)

T.P. Ryan / Environment International 28 (2002) 83–96

Balanus balanoides

Np

CFs

Pu Phylum

Genus

CFs

Myt. edulis

(SP) 140 – 260[13] (FM, TSW) (SP) 3.9k – 8.3k[13] (FM, FSW1) (SP) 1100 [15] (FM, FSW1) (SP) 380 – 490 [14] (FM, UC) 27 – 70 (25 days)[8] (LM, CFSW, NE) 70[9] (FM, TSW)

Myt. galloprovincialis Nuc. lapillus

Pat. vulgata

Gib. umbilicalis Spisula P. maximus

Buccinum O. vulgaris

Softshell clam (general)[17] Oyster (general) [17] [17]

[17]

Molluscs (general) Shellfish (general) [18]

Echinodermata

Asterina gibbosa

(SP) 110 – 450[13] (FM, TSW) (SP) 27k – 47k[13] (FM, FSW1) (SP) 13k [15] (FM, FSW1)

(SP) 15k [15] (FM, FSW1)

(SP) 1800 [15] (FM, FSW1)

(SP) 14k[15] (FM, FSW1)

(SP) 31k [15] (FM, FSW1)

(SP) 82 – 270 [13] (FM, TSW) (SP) 20k – 28k[13] (FM, FSW1) (SP) 5.9k – 41k [15] (FM, FSW1)

(SP) 57k [15] (FM, FSW1)

Cf

15 – 20 (92 days)[25] (LM, CFSW, NE) (SP) 46 – 118 [27] (FM, TSW) (SP) 580 [15] (FM, FSW1) (SP) 139 – 355 [27] (FM, TSW) (SP) 26 – 890 [15] (FM, FSW1)

(SP) 232 – 591

Aporrhais pespelicani

Whelk (general) Busycon

Np

[27]

(FM, FSW2)

270[14] (FM)

T. decussatus

Scallop (general)

Cm

T.P. Ryan / Environment International 28 (2002) 83–96

(SP) 3300 [15] (FM, FSW1) (SP) 65 – 170 [13] (FM, TSW) (SP) 1.8k – 4.1k[13] (FM, FSW1) (SP) 0.65k – 7k [15] (FM, FSW1)

Am

140 (17 days)[10] (LM, CFSW, NE) 110 (21 days)[10] (LM, CFSW, NE) (SP) 750 [14] (FM) 46[18] 65 (15 days)[6] (LM, CFSW, NE) (SP) 440 (FM, TSW) (SP) 100 – 160 (FM, TSW) (SP) 410 – 690 (FM, TSW) (SP) 140 (FM, TSW) (SP) 300 – 400 [14] (FM, UC) 1000[16] (UC) 200 (UC) 140 (FM, TSW) 3000 (UC) 452[9] (FM, TSW)

140 (38 days)[23] (LM, GWFSW, NE) 320 (20 days)[10] (LM, CFSW, NE) 550 (21 days)[10] (LM, CFSW, NE)

330 (20 days)[10] (LM, CFSW, NE)

35 (15 days)[6] (LM, CFSW, NE)

2000[16] (UC)

2000[16] (UC)

1000[16] (UC)

2000[16] (UC)

670 (FM, TSW) 20,000 (UC)

30,000 (UC)

400 (UC)

20,000 (UC) (continued on next page) 87

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Table 1 (continued ) Pu Phylum

Genus

CFs

Oph. texturata

310 (21 days)[10] (LM, CFSW, NE) 550 (10 days)[5] (LM, CFSW, NE) 2200[5] (FM, UC) 1830 – 2750[14] (FM, UC) 7 (21 days)[10] (LM, CFSW, NE)

Coscinasterias tenuispina Asterias ribens Sti. regalis Antedon mediterranea

(sub) Urochordata

Cnidaria

Annelida

1020 (FM, TSW) 760 (FM, TSW)

General

1370[9] (FM, TSW) 2100[17] (FM, TSW)

Cm

20 (21 days)[10] (LM, CFSW, NE) 173 (14 days)[21] (LM, NFSW, E)

496 – 1264[27] (FM, FSW2)

443 – 1127[27] (FM, FSW2)

Ascidians (general) Halocynthia papillosa

785[9] (FM, TSW)

General Actinia equina

165[9] (FM, TSW)

Are. marina

N. diversicolor

Marine worm (general)[17]

Cf

60 (21 days)[10] (LM, CFSW, NE)

Dendrodoa grossularia

General N. diversicolor (ex mucus prior to exposure) Her. hystrix

Np

193 (14 days)[21] (LM, NFSW, E)

130 (21 days)[10] (LM, CFSW, NE) 7 (21 days)[11] (LM, FSW2, UC) 103[9] (FM) 200 (15 days)[8] (LM, CFSW, NE) 190 (25 days)[12]

45 (21 days)[7] (LM, NFSW, E) 65 (21 days)[7] (LM, NFSW, E) 1000 (21 days)[10] (LM, CFSW, NE) 20 (20 days)[22] (LM, FSW2, UC)

40 (20 days)[22] (LM, FSW2, NE) 80 – 190 (12 days)[7] (LM, NFSW, E)

763 (21 days)[28] (LM, NFSW, E) 20 (20 days)[22] (LM, FSW2, UC)

2 (13 days)[26] (LM, FSW2, UC) 211 – 536[27] (FM, FSW2)

40 (20 days)[22] (LM, FSW2, NE)

315[9] (FM, TSW) 4100 (FM, TSW)

Key to data: LM = laboratory experimental measurement; FM = field measurement; E = equilibrium/approaching equilibrium/steady state; NE = nonequilibrium; FSW1 = filtered seawater (< 0.22 mm); FSW2 = filtered seawater (< 0.45 mm); CFSW = cotton-filtered seawater; NFSW = net-filtered seawater (< 43 mm); GWFSW = glass wool-filtered seawater; TSW = total seawater; SP = animal soft parts; UC = unclear (may refer to filtration or equilibrium). Key to references: [1] Guary and Fowler (1981); [2] Clifton et al. (1983); [3] Swift and Pentreath (1988); [4] Hayashi et al. (1990); [5] Guary et al. (1982); [6] Guary and Fowler (1982); [7] Carvalho and Fowler (1984); [8] Fowler et al. (1975); [9] Guary and Fraizier (1977); [10] Grillo et al. (1981); [11] Miramand et al. (1982); [12] IAEA (1985a); [13] Pentreath (1984); [14] Bowen et al. (1976); [15] IAEA (1985b); [16] IAEA (1978); [17] Noshkin (1972); [18] Kurabayashi et al. (1979); [19] Carvalho and Fowler (1985a); [20] Fowler and Heyraud (1974); [21] Fowler and Carvalho (1985); [22] Miramand et al. (1987); [23] Miramand et al. (1991); [24] Guary and Fowler (1978); [25] Guary and Fowler (1977); [26] Germain et al. (1987); [27] Germain and Pinte (1990); [28] Fowler et al. (1986); [29] Hamilton et al. (1991); [30] Fowler and Guary (1977); [31] Galey et al. (1983); [32] Aston and Fowler (1984); [33] Vangenechten et al. (1983); [34] Murray and Renfro (1976); [35] Beasley and Fowler (1976); [36] Germain et al. (1984). a Data refer to whole animals unless otherwise stated.

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Porifera (sponges)

Starfish (general)[17] Brittle stars (general)[17] Halichondria panciea

Am

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Table 2 Sediment – animal concentration ratios Phylum Arthropoda Mollusca

Annelida

Pua

Genus C. volutator Cir. borealis V. decussata Scr. plana Lit. lithorea N. diversicolor

Are. marina

Her. hystrix

Ama [11]

0.1 (4 – 14 days)

0.006 (20 days)[33] 0.01 (7 – 14 days)[11] 0.004 (2 days)[3] 0.001 (25 days)[34] 0.0015 (40 days)b[35] 0.0012 (40 days)c[35] 0.006 (14 days)[36] 0.002 (14 days)[36] 0.002 (6 – 14 days)[11] 0.05 – 0.12 (40 – 50 days)[33]

Cf a [11]

0.12 (14 days) 0.006 – 0.02 (40 – 50 days)[33] 0.004 – 0.002 (40 – 50 days)[33] 0.008 (7 – 14 days)[11]

0.0018 – 0.011 (10 – 12 weeks)[28]

0.0003 (40 days)b[35] 0.006 (40 days)c[35] 0.002 (14 days)[36] 0.002 – 0.005 (14 days)[36] 0.003 (6 – 14 days)[11] 0.05 (20 days)[33]

0.017 – 0.092 (10 – 12 weeks)[28]

Refer to Table 1 for key to references. a Exposure time is given in (brackets). b Sediment from Bravo Crater. c Sediment from Windscale.

Once assimilated, radionuclides are available for distribution throughout the animals body tissue. Clearly, the pattern of distribution will depend on the chemical properties of the ingested radionuclide, the physical and chemical form of the radionuclide when ingested, and the physiology of the host animal. Data for six arthropods, six molluscs, four echinoderms, two annelids, and one cnidarion are presented in Table 4.

biological half-time is influenced by these pools. This is manifested in the form of elimination patterns which are biphasic or even triphasic in character with distinct biological half-times for each phase. When moulting occurs in an animal, the elimination pattern can be greatly altered. The biological half-times for six arthropods, seven molluscs, two echinoderms, three annelids, one urocordat, and one cnidarion are presented in Table 5.

2.4. Radionuclide elimination

2.5. Chemical and physical speciation of ingested radionuclides

When a radionuclide is assimilated by an animal and distributed to the animal’s tissue, it is generally not locked into that tissue permanently. Instead, the animal will turn over the nuclide and excrete it after a period of time. The time required by the animal to eliminate half of the original amount of the radionuclide from its body is the biological half-time (Tb1/2). In practice, radionuclides are retained more effectively by different body organs creating distinguishable pools of radioactivity within the animal. The

There are many difficulties in performing experiments structured to evaluate the importance of chemical speciation in particular on the fate of a radionuclide in an animal. The preparation of the tracers required can cause problems particularly if a radionuclide exists in different chemical states in nature simultaneously as is the case for plutonium. Furthermore, it is possible that the host animal will modify the species of radionuclide as it passes through the body.

Table 3 Transuranic assimilation efficiencies in some marine invertebrates from ingested food Phylum

Genus

Element

Assimilation efficiency (%)

Labelled food

Arthropoda

Lys. seticaudata Car. maenas Car. maenas G. strigosa Cir. borealis

Mollusca

O. vulgaris L. littorea Oph. texturata

Plutonium Plutonium Californium Americium Americium Californium Americium Plutonium Californium Americium Americium Californium Americium

 15[8] 20 – 60[30] 23[28] 58[21]  5[19] < 5[19] 33[6]  7[3] 97[28] 87[21] 82 – 88[31] 91 – 98[31] 70 – 80[5]

Artemia N. diversicolor N. diversicolor Artemia salina Fish muscle/mussel soft parts Fish muscle/mussel soft parts Car. maenas Fuc. spiralis Mussel Mussel Mussel/clam Mussel/clam Mussels

Echinodermata

Mar. glacialis Starfish (general) Refer to Table 1 for key to references.

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Table 4 Percentage distribution of transuranic nuclides within the carcasses of marine invertebrates after exposure to labelled food/sea water Phylum

Genus

Element

Arthropoda

Car. maenas[30]

Pu

G. strigosa[7]

Can. pagurus[24]

Pil. hirtellus[28]

Lys. seticaudata[24]

Cir. borealis[19]

Mollusca

O. vulgaris[6]

L. littorea[3]

V. decussata[28]

Scr. plana[22]

Tissue

Hepatopancreas Shell Muscle and gill Am Exoskeleton Gill Muscle Gonads Hepatopancreas Digestive tract Haemolymph Np Exoskeleton Gills Epidermis Hepatopancreas Gut Haemolymph Muscle Ovaries Cf Exoskeleton Gills Gut Hepatopancreas Ovaries Muscle Haemolymph Remainder Np Exoskeleton/gills Eyes/stalks Muscle Hepatopancreas/gut Pu(IV)/Pu(V)/Am/Cf Exoskeleton Gut Digestive gland Muscle Haemolymph Pu/Am Branchial hearts Hepatopancreas Ventricle Gonad Kidney Digestive tract Gill and branchial gland Mantle — epithelium Mantle — mussel Remainder Pu Shell Head, foot, operculum Digestive glands, stomach Kidney Mantle + gill Mantle + rectum Remainder Cf Shell Mantle Muscle Gills Viscera Pallial fluid Cm/Am/Pu Soft part Shell Pallial fluid

% of total radioactivity

Uptake path (exposure time/post exposure)

43 – 85 8 – 43 5 – 10 88.1 2.3 1.7 4.3 0.3 6.1 0.1 98.1 0.39 0.1 0.9 0.026 0.12 0.33 0.013 80 2.4 0.8 3.6 1.7 2.3 6.4 3.5 92.7 0.21 1.6 5.5 41/63/90.4/79 13/9/4.7/5.2 16/5/1/4 12/16/2/5.1 18/7/1.9/6.7 40.6/72.8 2.2/1.3 – 0.1/0.1 0.1/0.5 0.5/1.2 18.3/3.8 3.4/0.4 1.8/0.6 33.0/19.3 82.5 5.1 7.6 0.3 0.3 0.6 0.8 67.3 4.9 1.0 5.5 9.8 11.5 19/12/9 80/87/89 1/1/1

Labelled food

Labelled seawater (21 days)

Labelled seawater (48 days)

Labelled seawater (23 days)

Labelled seawater (50 days)

Labelled seawater (NA)

Labelled seawater (50 days)

Labelled seawater (23 days)

Labelled seawater (NA)

(continued on next page)

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Table 4 (continued ) Phylum

Genus

Element

Tissue

% of total radioactivity

Uptake path (exposure time/post exposure)

Scr. plana[22]

Am/Pu

Cm/Am/Pu

58/66 36/30 5/4 32/57/16 61/36/80 6/7/4 91.6/91.2 3.3/6.3 1.6/0.9 2.8/1.1 0.7/0.6 4.9 5.3 ND 92.9 7.5 14.9 77.6 ND 22.8/98

Labelled sediment

Cer. edule[22]

Shell Soft part Pallial fluid Soft part Shell Pallial fluid Shell Viscera Gills Mantle Muscle Central disc Arms Gonads Gut Central Disc Arms Gonads Gut Body wall Pyloric caeca Gut Coelomic fluid Body wall Pyloric caeca Gut Male gonad Female gonad Pyloric caeca Gut Gonads Tube feet Body wall Body wall Pyloric caeca Gut/gonad Body wall Internal tissues Atrial water Gonad Setae Body wall Gut Coelomic fluid Body wall Tentacles Mesogloea

65.1/1.2 12.1/0.6 ND/0.2 92.5 4.4 – 5 0.5 – 0.6 2.6 1.9 84.9/94.4 10.1/3.9 0.1/0.1 1.6/0.4 3.4/1.4 94.5 3.9 0.5/1.1 90.2 6.8 3.3 1.1 49 47 0.2 3.9 75 11 14

Myt. galloprovincialis Np[24]/Am[1]

Echinodermata

Oph. texturata[28]

Cf

Am[21]

Cos. tenuispina[5]

Pu

Mar. glacialis[5]

Pu

Mean values[31]

Am/Cf

Asterias rubens[5]

Pu

(sub) Urochordata Halo. papillosa[24]

Am

Annelida

Her. hystrix[28]

Cf

Cnidaria

Act. equina[7]

Am

However, some experiments have been carried out and these are discussed later.

3. Discussion 3.1. Seawater – animal CFs for marine invertebrates As the data compiled from the literature in Table 1 demonstrate, a number of interpretations of the CF have emerged, making comparison between computed CFs very

Labelled seawater (NA)

Labelled seawater (NA)

Labelled food, 37 days postingestion

Labelled sea water, 113 days postexposure

Labelled food, 34 days postexposure/seawater, 10 days postexposure

Field measurement

Field measurement

Labelled seawater (22 days)

Labelled seawater (23 days)

Labelled seawater (21 days)

difficult. Some authors use a CF which is the ratio between the concentration of the radionuclide in the whole animal and that in the seawater. Others only consider the soft parts of the animal. Some authors use unfiltered seawater for their calculation while others use filtered seawater. Of those that use filtered seawater, there is a divergence of filtering methodologies. The range of filtering systems include: cotton wool, glass wool, plankton nets (< 43 mm), and membrane filters of various pore sizes (< 0.45 and < 0.22 mm). Some CFs quoted are those derived from field measurements while others are the results of laboratory

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Table 5 Transuranic elimination rates from marine invertebrates Phylum

Genus

Element

No. of phases identified

Biological half-times (Tb1/2, days)

Uptake medium

Arthropoda

Pil. hirtellus[28] Car. maenas[28] Lys. seticaudata[28] G. strigosa[21] G. strigosa[7] Gam. locusta[7] Cir. borealis[19] O. vulgaris[6] O. vulgaris[6] V. decussata[28] V. decussata[32] V. decussata[32] L. littorea[3] L. littorea[3] L. littorea[3] T. decussatus[10] T. decussatus[10] T. decussatus[10] Apo. pespelicani[10] Apo. pespelicani[10] Myt. galloprovincialis[8] Myt. galloprovincialis[8] Myt. galloprovincialis[1] Myt. galloprovincialis[1] Myt. galloprovincialis[1] Myt. edulis[2] Myt. edulis[2] Myt. edulis[2] Myt. edulis[2] Myt. edulis[2] Oph. texturata[28] Oph. texturata[10] Oph. texturata[10] Sti. regalis[10] Sti. regalis[10] Her. hystrix[28] Her. hystrix[32] Her. hysterix[10] Her. hysterix[10] Ant. mediterranean[21] N. diversicolor[8] N. diversicolor[7] N. diversicolor[8] N. diversicolor[8] Halo. papillosa[21] Act. equina[7]

Cf Cf Cf Am Am Am Pu[III,IV] Pu/Ama Am Cf Pu Pu Pu Pu Pu Cm Am Pu Am Pu Pu(VI) Pu(IV) Am Pu(IV) Pu(VI) Pu Am Pu[V,VI] Am Cf Cf Am Pu Am Pu Cf Pu Pu Am Am Pu(VI) Am Pu Pu Am Am

2 2 Moulting 1–2 3 2 2 2 2 2 1 1 2 2 2 2 2 2

R; 50 2; 18

Seawater Labelled food Seawater Labelled food Seawater Seawater Seawater Seawater Labelled crab Seawater Seawater Sediment Seawater Labelled seaweed Silt Seawater Seawater Seawater

Mollusca

Echinodermata

Annelida

(sub) Urochordata Cnidaria

2 >1 3 3 3 2 2 2 2 2 1 2 2 3 2 2 2 2 2 2 >1 3 3 1 3 2

R; 14 0.6; 7; 139 6; 38 < 4.4; 60 2; 560 17; 160 R; 126 50 24 10; 193 1; 69 1; 69 7; 53 6; 80 7; 62 as for T. decussatus as for T. decussatus 7; 776 39 11; 22; 480 2; 10; 193 1; 13; 192 1.8 h; 708 days 0.9 h; 303 days < 4.4; 87 < 4.4; 261 < 4.4; 288 36 < 1; 313 < 1; 410 < 1; 6; 68 4; 130 R; 50 1.3; 54 R; 66 R; ? 0.4; 51 79 0.4; 24; 368 1.3; 7; 54 24 1; 7; 83 0.1; 47

Seawater Phytoplankton suspension Seawater Seawater Seawater Seawater Seawater Seawater Seawater Labelled food Seawater Seawater Seawater Seawater Seawater Seawater Seawater Seawater Seawater Seawater Seawater Sediment Seawater Seawater

R: Rapid phase. a Similar behavior after 10 days exposure.

experimentation. Of the CFs derived from laboratory experimentation, differences emerge in the length of time to which animals are exposed to labelled seawater and, in many cases, a steady-state situation is not reached over the duration of the experiment. Some authors have estimated CFs in terms of the biologically available fraction and have examined the concentration of the radionuclide in its chemical species computing separate CFs for different oxidation states. However, many of the experiments reported were designed to determine the relative importance of uptake pathways which quite expectedly will result in a

divergence of experimental conditions and lead to a divergence in computed CFs. Other parameters can also influence the measured CFs such as the degree of thoroughness in cleaning animals of sediment and the presence or removal of mucus or bysuss treads. While there is a divergence of formulations of the CF, the main issue of contention is whether or not the CF should be reported using filtered or unfiltered seawater. In field studies, the magnitude of CFs reported on the basis of unfiltered seawater can be influenced by fluctuations in the quantity of suspended material, and hence, fluctuations in available

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contaminant as a result of weather conditions, turbidity, and algae activity. In laboratory experiments, the situation is somewhat different in that there is control over the initial conditions. For example, filtered or unfiltered seawater could be used. However, as the experiment progresses, the quantity of suspended material will be modified as the animal under study excretes ingested material which may not be as easily diluted with its surroundings as would be likely to happen in the environment. Furthermore, authors sometimes express the activity concentration in seawater in terms of becquerel per milliliter as opposed to becquerel per gram resulting in admittedly small differences in CF due to water density. While there is no simple resolution of these conflicts, one useful step forward would be the promotion of a reporting system for seawater – animal CFs. It is suggested that while Eq. (1) should form the basis of the definition of a seawater – animal CF for marine invertebrates, the reported value should be accompanied with the following additional information: (1) the depuration time prior to measurement; (2) details of other cleansing procedures; (3) the presence or absence of mucus or byssus tread attachments; (4) a clear distinction should be made between field and laboratory measurements and in the latter case the species of radionuclide used should be reported if known; (5) it should be clearly stated whether or not the animal organs or the whole body of the animal was used in the measurement and information about the wet and dry weight of the animal or animal part; (6) an estimate of the degree of equilibrium between the animal and its environment should be given if possible and certainly in the case of a laboratory experiment, the exposure time of the animal should be quoted; and (7) it should be clearly stated whether filtered or unfiltered seawater was used in the measurement. In the situation where filtered seawater was used, the filtering methodology should be reported. 3.1.1. Seawater – animal CF data Where data coincide, there is a strong tendency for seawater – animal CFs to be higher for americium than plutonium (Table 1). A notable exception to this is for the echinoderm Ophiura texturata where the CF for plutonium is 310 as opposed to 60 for americium. A similar result is also found for the annelid N. diversicolor where plutonium uptake is more pronounced than that of americium. It is well established that the behavior of americium and curium is comparable. This is reflected in their similar behavior in animals such as the arthropod C. volutator, the molluscs Cerastoderma edule, Tapes decussatus, and the annelids A. marina and N. diversicolor where the seawater –animal CFs reported are very similar. However, some differences in CFs for americium and curium are reported for the molluscs S. plana (whole animal), Nucella lapillus (soft parts), and Patella vulgata (soft parts) though these may not be significant in the context of the overall experimental uncertainties or may be partially explained in terms of differences in experimental parameters such as animal exposure time.

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3.1.2. Field studies versus laboratory studies Differences between CFs derived in the laboratory and those derived in the field are in evidence. For example, the field measurements made on the annelid A. marina yielded CFs in the range 211 – 536 (Germain and Pinte, 1990), while the laboratory experiments yielded a CF of only 2 (Germain et al., 1987). A similar pattern was found for plutonium in the same animal with a laboratory-derived CF of 7 (Germain and Pinte, 1990) and a field measurement of 103 (Guary and Fraizier, 1977). It is not unreasonable to expect significant differences between field and laboratory studies. In general, studies in the laboratory are concerned with specific uptake pathways, whereas in the field, measurements take account of all of the vectors involved including site-specific environmental parameters which may give rise to local variations in seawater – animal CFs. 3.2. Transuranic uptake from sediment Laboratory studies by Hamilton et al. (1991) demonstrate that there is initially a preferential uptake of plutonium over americium from sediment by biological systems but that this may change over longer sediment – animal exposure times. They also found that americium bioavailability can be source dependent. In particular, they found that americium in the sediments taken from Thule in Greenland is more biologically available than that from sediments contaminated by nuclear weapons testing or reprocessing activities. They also assert that some of the differences between laboratory-derived CRs and those estimated in the field may be due to residual sediment in the gut of the animals sampled in the field and pointed to this as a factor to be cautious about in performing such experiments. While the CRs for californium and other transuranics are low, one possible transfer mechanism is suggested. It has been noted that generally the gut of invertebrates is acidic and this can cause leaching of transuranics from sediments during their passage through the gut. The transuranics are subsequently taken up by the animal’s blood stream and assimilated into tissue. However, Fowler et al. (1986) noted that the close agreement between CFs based on interstitial water of sediment and those for seawater uptake experiments suggests that most of the californium accumulated from sediment in their experiment was derived from interstitial water as opposed to directly from ingestion of the sediment. Similar observations were made for plutonium and americium (Miramand et al., 1982; Germain et al., 1984). 3.3. Transuranic uptake from food and tissue distribution post exposure The transuranic assimilation efficiencies for invertebrates are generally high ranging between 5% for americium in the arthropod Cir. borealis and 98% for californium in the echinoderm Marthasterias glacialis (Table 3). These assim-

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ilation efficiencies are high in comparison to plutonium uptake by plaice (Pleuronectes platessa) at < 1% (Pentreath and Lovett, 1976) and 241Am in teleost fish (Carvalho et al., 1983) at 0.7% or by mammals in general at < 0.1% (Stara et al., 1971). The distribution of transuranics in the tissues of marine invertebrates is strongly dependent on the uptake pathway. Distribution within the body is more likely when the transfer vector for radionuclides is ingestion with food. However, when the vector is labelled seawater, the preponderance of the nuclide assimilated by animals with an exoskeleton or shell is on that exterior surface. Among the arthropods exposed to labelled seawater for periods of time ranging between 20 and 50 days (G. strigosa, Cancer pagarus, Lys. seticaudata, Pilumnes hirtellus, and Cir. borealis), more than 80% (on average) of the transuranics were associated with the exoskeleton or shell (Table 4). A similar situation prevails among the molluscs examined where greater than 50% of americium, plutonium, neptunium, californium, and curium was associated with the animals’ exterior with the exception of americium in the mollusc Cer. edule where only 36% was deposited on the shell. Echinoderms exposed to transuranic elements in labelled seawater accumulate the vast bulk of the nuclides in the body wall with a similar pattern emerging for the annelids and the cnidarions examined. Indeed, a study relating the salt content (CaCO3) of the body wall with americium uptake showed a positive correlation (Fowler and Carvalho, 1985). A similar relationship between plutonium uptake and the level of tissue calcification in a number of marine species has been reported (Guary and Fraizier, 1977). Furthermore, studies have shown that transuranics have an affinity for mucus secretions and similarly for bysuss treads (Guary et al., 1982; Fowler et al., 1975).

long-lived pool of plutonium is eliminated with a Tb1/2 of 130 days but the long-lived component of americium is eliminated much quicker with a Tb1/2 of 68 days. The behavior of plutonium and americium in the mollusc O. vulgaris was found to depend on the exposure time of the animal to the labelled seawater. The authors suggest that after a longer exposure time, the americium turnover rate slows down in comparison to plutonium. A further study carried out with the mollusc T. decussatus (Grillo et al., 1981), where the animal was exposed to three different nuclides namely, americium, curium, and plutonium, demonstrated that all three nuclides are eliminated in a biphasic mode but the Tb1/2 for the long-lived components of americium and curium were slightly different at 80 and 53, respectively. In the cases studied (Carvalho and Fowler, 1985b; Guary and Fowler, 1981; Fowler and Carvalho, 1985; Swift and Pentreath, 1988), transuranics were turned over in the animals much faster when introduced via labelled food as opposed to when the animals were exposed to labelled seawater. A partial explanation for this is that much of the activity taken up from labelled seawater will be associated with the exoskeleton or shell and the turnover of this component is very slow. One exception to this is where moulting occurs as for the shrimp Lys. seticaudata which sheds its exoskeleton in a periodic moulting phase. The longest turnover time found was for plutonium in the mollusc Mytilus galloprovincialis which had a Tb1/2 of 776 days after exposure to labelled seawater (Fowler et al., 1975). The shortest turnover time for a ‘‘long-lived’’ pool was found to be the arthropod G. strigosa with a Tb1/2 of 14 days after exposure to americium-labelled food (Fowler and Carvalho, 1985). 3.5. Speciation effects

3.4. Transuranic elimination from marine invertebrates The elimination of transuranics from most species examined (Table 5) conforms to a standard biphasic exponential model as described by Comar (1955). However, in a number of cases, three phases of elimination were identified. Americium is lost from the squat lobster G. strigosa from three distinct radionuclide pools with biological half-times (Tb1/2) of 0.6, 7, and 139 days, respectively, after exposure to labelled seawater (Carvalho and Fowler, 1984). The echinoderm Stichopus regalis eliminates americium in a similar fashion with half times of < 1; 6 and 68 days also after exposure to labelled seawater (Grillo et al., 1981). A third example is that of the annelid N. diversicolor which eliminates both plutonium and americium in a triphasic mode (Fowler et al., 1975; Carvalho and Fowler 1984). The relative retention of individual nuclides varies from species to species. In the case of the annelid N. diversicolor, the longer-lived component of americium is eliminated with a Tb1/2 of 368 days as opposed to Tb1/2 of 54 days for plutonium. In the case of the echinoderm Sti. regalis, the

Plutonium can exhibit four different oxidation states in seawater simultaneously. These states are usually grouped in terms of the reduced fraction [Pu(III, IV)] and the higher oxidised fraction [Pu(V, VI)]. The Pu(III, IV) group is generally associated with the sedimentary or suspended marine material while the Pu(V, VI) is associated with that fraction which is considered to be in solution. Americium is considered to exist in seawater as Am(III) and is largely associated with particulate matter exhibiting high Kd (particle – water distribution coefficient) values. Likewise, curium is thought to be present in seawater as Cm(III) with similar Kd values to those of americium. Neptunium occurs in seawater mainly in the pentavalent state (Np(V)) as the monovalent neptunyl cation NpO2+ and is less particle reactive than plutonium, americium, or curium. However, work by Germain et al. (1987) demonstrates the existence of complex anionic or neutral forms possibly associated with particulate material. Fowler et al. (1986) suggest that californium has a high affinity for particulate material and probably exists in aqueous solutions as Cf (III).

T.P. Ryan / Environment International 28 (2002) 83–96

Most of the studies examined in this review deal with chemical speciation only as an initial condition in the preparation of tracer solutions. A small number of publications actively look at the effect of variations in chemical speciation on uptake rates in marine organisms. Fowler et al. (1975) observed that the turnover of 237 Pu(III, IV) in mussels appeared much faster than in mussels which had accumulated the Pu(V, VI) although they were unable to be definitive in their conclusions due to the nature of the experimental design. However, Carvalho and Fowler (1985a) found that the marine isopod Cir. borealis accumulates Pu(V) from seawater slightly faster than Pu(IV). In a study on the uptake of plutonium from labelled seawater by clams (Venerupis decussata), Aston and Fowler (1984) did not attach significance to small differences in uptake they observed for the two groups of chemical species of plutonium Pu(III, IV) and Pu(V, VI). They found that after a 22-day exposure to seawater, the plutonium CFs for V. decussata were 74 ± 5 and 61 ± 1 for Pu(III, IV) and Pu(V, VI), respectively. Similarly, they found the CFs to the annelid Hermione hysterix to be 370 ± 10 and 275 ± 11 for the respective species. They found a similar lack of variation in the uptake by these animals of plutonium from interstitial water. However, Sibley and Sanchez (1986) suggest that as opposed to there being a lack of behavioral differences among chemical species, the chemical form may be continually undergoing transformations within the solution. Hamilton et al. (1991) attributed time-dependent changes in the bioavailability of plutonium and americium uptake to possible differences in biochemistry, physical, and chemical change and complexation of transuranics by animal excretions. Guary and Fowler (1978) suggest that differences between Pu and Np uptake in the exoskeleton of the crab Can. pagurus may be due to differences in the physical – chemical form of the nuclides in the environment. Observations on species differences for other nuclides are sparse. One study by Germain et al. (1987) on neptunium in labelled seawater found that in a system which had been labelled with the soluble cationic form of neptunium (NpO2+ ), there was no significant change in the chemical species over the experimental period.

Acknowledgments The author gratefully acknowledges the following for reviewing this manuscript and for providing useful suggestions in the course of its preparation: B. Rafferty, D. Pollard, S. Long, J.D. Cunningham, P. Germain, and F.P. Carvalho.

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