Natural-Series Radionuclides in Traditional Aboriginal Foods in Tropical Northern Australia: A Review

This paper gives a review of available information on natural-series radionuclides in traditional Aboriginal foods of northern Australia. Research on this topic has been carried out primarily for radiological impact assessment purposes in relation to uranium mining activities in the region. Many of the studies have concentrated on providing purely concentration data or concentration ratios, although more detailed uptake studies have been undertaken for freshwater mussels, turtles, and water lilies. The most-studied radionuclides are U and Ra. However, dose estimates based on current data highlight the importance of Po, particularly for the natural (nonmining-related) dose. Data on uptake by terrestrial flora and fauna are scarce in comparison with aquatic organisms, and this knowledge gap will need to be addressed in relation to planning for uranium minesite rehabilitation.


INTRODUCTION
This paper gives a review of available information on natural-series radionuclides in traditional Aboriginal foods of northern Australia. Research on this topic has been driven by the coincidence of a number of factors. These include: the presence of uranium mining activities over several decades, particularly within World Heritage listed Kakadu National Park and western Arnhem Land, areas which are occupied by Aboriginal people living a semi-traditional lifestyle; the monsoonal tropical climate of the region; early experience of environmental problems resulting from acid mine drainage at the Rum Jungle mine; and recommendations for research made by the Ranger Uranium Environmental Inquiry [1]. The primary focus of the research has been on providing information useful for radiological impact assessment purposes, particularly in relation to intake of uranium series radionuclides by Aboriginal people. nickel, zinc, and manganese). The Australian Government undertook remediation of the site during the 1980s, and monitoring of the site is continuing [3].
Several prospects were mined in the South Alligator Valley in and around what is now known as Stage 3 of Kakadu National Park. The first of these prospects was discovered in 1953 [4]. There were two treatment plants in the area drawing upon ore from different mines [5].
In 1958, United Uranium purchased the North Hercules gold plant at Moline, 50 km east of Pine Creek (about 65 km from the South Alligator mines). The plant was commissioned with an annual capacity of about 130 tonnes U 3 O 8 in May 1959 [5].
In 1970, a uranium orebody was discovered at Nabarlek 15 km east of Oenpelli (Gunbalanya), near Cooper Creek (a tributary of the East Alligator River). The Nabarlek 1 orebody was mined out in just over 4 months during the dry season of 1979. With an average ore grade of 2%, 600,000 tonnes of ore were stockpiled with processing beginning in 1980 and continuing for the next 9−10 years [5].
Ranger is the only operating uranium mine in the Top End at present. The Ranger orebodies #1 and #3 are about 1,200 m apart, and are situated near Magela Creek, a tributary of the East Alligator River. Mining of Ranger #1 occurred between 1980 and 1994 using an open-cut method. Complete mining of approximately 20 million tonnes of ore from this orebody at an average grade of 0.327% required the removal of about 60 million tonnes of waste rock and very low-grade mineralised material. Open-cut mining of Ranger #3 commenced in 1997 and milling of this ore is expected to continue to 2014. Fig. 3 shows the region around the Ranger minesite, where much of the sampling for studies discussed in this paper has occurred.
The Koongarra prospect lies some 30 km south of Ranger. The upper orebody has proved and probable ore reserves containing 14,500 tonnes of uranium oxide with an average grade of almost 0.8% U 3 O 8 . This ore would be accessible by open-pit mining and there is associated gold within the orebody [5].
The Jabiluka 1 uranium deposit was discovered in 1971. In 1973, further drilling located the larger Jabiluka 2 uranium orebody about 1 km to the east. Jabiluka lies on the edge of the Magela Creek floodplain, and is 20 km to the north of Ranger. Jabiluka 2 has reserves in excess of 160,000 tonnes of uranium oxide, and is one of the world's larger high-grade uranium deposits [5].

Climate
The climate is tropical monsoonal and characterized by intense rainfall during the wet season (November to April), followed by an almost rainless dry season (May to October). At Jabiru airport, the mean annual rainfall and annual pan evaporation recorded between 1971 and 1998 were 1,480 and 2,615 mm, respectively [6]. Almost 96% of rainfall occurs in between November and April and almost 60% in the 3 months of January, February, and March.
The Inter Tropical Convergence Zone extends into Northern Australia in the summer months, characterized by the inland of Australia being intensively heated resulting in a flow of tropical maritime air over the region [7] producing strong convective rainfall. These convective storms result in highintensity rainfalls for short periods of time during the wet season. The wet season monsoonal winds originate in equatorial regions and move in from the northwest across the coast bringing hot, humid, unstable conditions. Thunderstorms can be common along the coast with an average of 60-80 thunder days each year, which become less frequent further south [8]. Monsoonal depressions cause heavy rains and tropical cyclone activity.

Traditional Aboriginal Foods and Estimation of Radiological Impact
Aboriginal people of northern Australia obtain food by a combination of commercial purchases (primarily of items imported from outside the region) and customary harvesting of both native and introduced flora and fauna ("bush foods"). In an anthropological study carried out in 1979-80 at Momega in western Arnhem Land, Altman [9] found that 46% of total kilocalories and 81% of total proteins came from bush foods. He identified over 80 floral species used as bush foods, and in total 170 species of flora and fauna were observed being consumed. The majority of these are native species that are not used in agriculture, and so very little information on element or radionuclide concentrations in the edible portions is available. A sample of a single species will generally have several edible parts (e.g., various organs of an animal). For some species, Aboriginal people may reserve different parts of the animal or plant for different people. The reasons for this may include land ownership, social standing in the clan, age group, gender, and personal totem responsibilities.
Taking into consideration the number of radionuclides that could be important from a dose assessment perspective (these include isotopes of uranium, thorium, radium, lead, polonium, and actinium), it can be seen that the full matrix of bioaccumulation pathways that are of interest is very large. In the case of work undertaken in the ARR over the last 2 decades, researchers have generally addressed this problem by taking one or more of the following approaches: • Initially targeting aquatic organisms, as these were expected to be the most important during the operational phase of uranium mining. • Undertaking detailed radionuclide uptake studies on radionuclides and species for which there is evidence that they are important from a dose perspective (in particular uptake of 226 Ra by freshwater mussels, turtles, and water lilies). • Using the concentration ratio approach to assess other radionuclide/bush food combinations.
• Carrying out long-term monitoring of specific radionuclide/food combinations. Such monitoring has been primarily carried out by the mining companies [10].
The concentration ratio (CR) or concentration factor (CF) method of dose assessment has been discussed in detail elsewhere [11,12,13,14,15]. The CR for a radionuclide in an organism is defined as the activity of the nuclide per unit weight of the organism, divided by the activity of the same nuclide per unit weight of substrate, where the substrate is the physical medium (e.g., water, food, or soil) from which the organism obtains the nuclide. Deficiencies in the CR approach are known to exist but, in general, its use is likely to be conservative provided locally derived values are used.
Comparison of concentration and CR data between different studies is not always possible because there is no standard either for the substrate or for the form of the analysed tissue or substrate (i.e., fresh weight or "wet weight" vs. dry weight of tissue; total vs. filtered water sample; wet vs. dry sediment or soil sample). It is important that researchers explicitly state this information in their reports in order that the data can be properly assessed and utilised.

Water Lily (Nymphaea species)
Water lilies from the genus Nymphaea are widespread and common in the Top End, typically growing in seasonally inundated areas with a water depth to about 2 m [16]. They are abundant in the floodplain backwater swamps and billabong fringes of the Magela Creek.
Accumulation of radionuclides by water lilies was recognised early as a potentially important pathway for radiological impact arising from releases of water from the Ranger mine [17]. Such accumulation can result from uptake from the water column (whether by absorption of dissolved radionuclides or deposition of fine suspended sediments or colloidal forms onto submergent surfaces) and uptake into roots and rhizome from the sediment in which the plant is rooted, with the possibility of subsequent translocation in the plant. Local Aboriginal people eat all parts of the plant including the rhizomes, flowers, seed heads, and certainly the stems, which are a favoured food [18].
Uptake of 226 Ra by Nymphaea sp. was the subject of a series of studies by Twining [19,20,21,22]. He found that 226 Ra concentrations in the root and rhizome are higher than in foliage, this being due primarily to surface accumulation. Little radium reached the pith of the rhizomes. Uptake of radium by the foliage was found to be primarily from the water rather than by translocation from the roots. For samples collected in the field, the distribution of radium and calcium concentrations in the foliage were strongly correlated. However, analysis of the ratio of radium to calcium in the plant, compared to extractable concentrations in the water and sediment, showed no correlation between foliage and supporting media, suggesting that different mechanisms were involved in accumulation of radium and calcium. In a laboratory experiment of uptake of 226 Ra to leaves from an artificial Magela Creek water, a CR of 3,600 L kg -1 dry weight (DW) was obtained [19]. Derived uptake and loss rate coefficients were 2.00 and 0.55 day -1 , respectively, although there was evidence of a second compartment for accumulation with a very low loss rate.
Pettersson et al. [23] measured concentrations of 234,238 U, 228,230,232 Th, 226 Ra, 210 Pb, and 210 Po in root, rhizome, and foliage of Nymphaea sp. as well as sediment and water samples from four billabongs (permanent waterholes) on the Magela Creek system in order to obtain CRs for these radionuclides. Comparing concentrations in water lily parts and concentrations in sediment and water, they obtained better correlations with the sediment and concluded that this is the primary source of radionuclides to the plant. Despite the fact that the radionuclides studied represented five different elements, there was only a small variation in the derived CRs. For example, in the case of foliage, the CRs (waterlily fresh weight to sediment wet weight) for the eight radionuclides ranged between 0.0045 (for 232 Th) to 0.014 (for 228 Th). For roots and rhizomes the derived CRs were of the order of 0.01 to 0.03.
Hancock [24] extended the Pettersson et al. [23] study by carrying out similar measurements for six individual plants and associated sediment from one billabong. His results were broadly consistent with those of Pettersson et al. [23], although the derived CRs were about a factor of 5−7 lower. For foliage, the CRs relative to sediment followed the element order Ra > Po > Pb > U ≥ Th, with about an order of magnitude difference between the CRs for Ra and Th.

Freshwater Mussels (Velesunio angasi)
A large number of studies have been conducted on the freshwater mussel, Velesunio angasi, in coastal streams of the Northern Territory, particularly populations from the Magela Creek system. Humphrey and Simpson [25] carried out a comprehensive study of the autecology of the species, including development of a method for age determination using annular dark rings in the shells, which has provided a base for many of the subsequent studies.
Early research showed that populations of V. angasi in the Magela Creek system had very high flesh concentrations of 226 Ra [26]. The species is also a significant food source for some local Aboriginal groups. Consequently, the potential radiological impact arising from release of uranium mine and mill waters in the region is believed to be dominated by radium uptake by mussels [27,28], and this has been the major reason for the research undertaken on radionuclide uptake mechanisms by this species.  [29]. Dry: fresh weight ratios for mussel flesh are generally in the range 0.08−0.15. ** Ca and Mg concentrations in billabong waters are ranges (no. samples) reported in [30] for the period 1978−1981; data for Cooper Creek were for Nimbuwah Billabong. *** Sediment results are for surface sediment samples collected by eriss over 1983−87, and analysed by gamma-ray spectrometry. Table 1 shows results for 226 Ra concentrations and 228 Ra/ 226 Ra ratios for samples collected from a number of locations in the ARR in 1983 (each sample comprised the combined flesh of a number of mussels [29]). These data show that the high 226 Ra concentrations are regional in nature rather than being confined to areas downstream of uranium mining operations. The 228 Ra/ 226 Ra ratios for mussels and sediments from the three billabongs immediately downstream of Ranger were lower than for mussels from other billabongs, however this is to be expected as the ratios for soils of the Ranger area are naturally low.
By contrast with the high 226 Ra and 228 Ra concentrations in mussel flesh, specific alpha activities measured for shells of mussels from Georgetown billabong were only of the order of 40-60 Bq kg -1 [31].
Radium is stored in calcium phosphate granules in the mussel flesh [32,33]. Radium is retained in these granules over long periods, resulting in a long effective biological half-life in the mussel tissue. As can be seen in Table 1, decay of accumulated 228 Ra (radioactive half-life = 5.75 years) over the life of the mussel results in lower 228 Ra/ 226 Ra ratios in mussel tissue than in the billabong sediment. Measurements and modelling of 228 Ra/ 226 Ra ratios vs. mussel age yielded an estimate for the radium biological half-life of 8.8 ± 1.0 years in mussels from Mudginberri billabong [34]. 226 Ra uptake rates are inversely proportional to both calcium and magnesium water concentrations [35]. Consequently, the high flesh radium concentrations in mussels from ARR creek systems are an outcome of the low calcium and magnesium concentrations in the water and the long biological half-life of radium in the mussel. This explains why the highest 226 Ra concentrations in mussels shown in Table 1 were obtained for Bowerbird, a billabong with low 226 Ra concentrations in the bottom sediments but also low calcium and magnesium concentrations in the water.
As a result of the long biological half-life, radium concentrations are positively correlated with mussel age, as well as with other age-correlated parameters such as shell length and tissue mass, and with concentrations of the alkaline earths calcium, magnesium, and barium [36,37,38,39]. Mussel size and sex have little or no effect on the rates of uptake of 226 Ra per gram of tissue [35].
The biological half-life for 210 Pb in V. angasi is long; one experimental study showed no significant reduction in tissue concentrations over 160 days [40]. As a consequence of this, plus the fact that there is some support from its 226 Ra progenitor, 210 Pb is accumulated in the tissue [34,38]. By contrast, the biological half-life for uranium is only of the order of a few days [41].
Concentrations of 210 Po in the mussel flesh are significantly higher than those of its progenitor 210 Pb [34], resulting in a high CR (see Table 2). Since the radioactive half-life of 210 Po is only 138 days, the high concentrations imply that uptake rates are high for polonium. Note: CRs relate to fresh weight of mussel tissue and total water concentration. Data from [27].
V. angasi show behavioural responses to elevated uranium concentrations in water, with declines in duration and amplitude of valve gape and increases in frequency of valve adductions having been observed at UO 2 concentrations greater than 350 µg L -1 in a synthetic Magela Creek water [42]. These valve movement responses are highly dependent on experimental conditions, with observed response endpoints varying over an order of magnitude for differing pH values and dissolved organic carbon concentrations [43].
In addition to its importance for radiological impact assessment, V. angasi is an important indicator species for other environmental and human health issues. These include bioaccumulation of chemical pollutants, its use in archival monitoring, and its use in laboratory and field sublethal effect studies [44,45]. As a result, this species is likely to remain a focus of efforts in monitoring and assessment of mining impact in Top End streams.

Other Aquatic Fauna
Some earlier data for edible aquatic fauna in the ARR were published by Davy and Conway [26] and Koperski and Bywater [10]. With the exception of data for freshwater mussels, the concentrations measured were generally lower than 1 Bq kg -1 (fresh weight) of flesh for individual radionuclides. Consequently, high-sensitivity radionuclide measurement techniques are required for studies of this nature.  [46]). In each case the data refer to fresh weight of flesh and total water concentration. The CR values range over two orders of magnitude, illustrating the fact that, in cases where the doses are of the order of magnitude of any relevant dose limits, more robust bioaccumulation estimation methods and/or monitoring regimes will need to be used. Jeffree [50] carried out laboratory-based experiments on uptake of 226 Ra by freshwater turtles, including snapping turtles (Elseya dentata) from Magela Creek, under varying calcium and magnesium water concentrations. He found that the capacity of E. dentata to accumulate 226 Ra from the aquatic medium was about two orders of magnitude less than that of tissue of V. angasi, in agreement with the results of the field-based studies discussed above (Tables 2 and 3). In contrast with the results of analogous experiments with the freshwater mussel V. angasi, for E. dentata increased calcium water concentrations did not significantly reduce 226 Ra uptake to soft tissues (with the exception of the skin), but significantly increased the 226 Ra concentration in bone and muscle. Increased magnesium water concentrations had a significant inverse effect on 226 Ra uptake in bone, muscle, skin, liver, and gut, but had no significant effect for uptake to the shell.

TERRESTRIAL FAUNA
There have been relatively few radionuclide studies on terrestrial animals in the Top End. Nonaquatic animals that have been investigated include the water buffalo (Bubalus bubalis), the pig (Sus scrofa) (both introduced species), and the magpie goose (Anseranas semipalmata). All three species spend much of their time in a floodplain environment.

Buffalo
The buffalo is a grazing animal with the bulk of its food coming from grass. The contribution of buffalo to Aboriginal diet has decreased markedly in recent years as a direct result of the national Brucellosis and Tuberculosis Eradication Campaign (BTEC) [51]. Tens of thousands of animals were eradicated during this program that took place from the mid 1970s and continued into the early 1990s, leaving feral buffalo numbers very low in the ARR for a number of years. Now some years after the BTEC has finished, buffalo numbers are increasing, particularly in eastern Arnhem Land [52]. Buffalo numbers are still low in Kakadu National Park [53] as a result of an active feral animal reduction program maintained by Parks Australia North. Data for uranium-series radionuclides from samples of buffalo, pig, and magpie geese that were collected in the ARR are available from several studies [10,26,46,47]. These studies showed that radionuclide activity concentrations were higher in kidney and liver than other parts of the animal, particularly for 210 Po (Table 4).

Pigs
Early European settlers introduced pigs into Australia and it was not long before large feral populations became established. Feral pigs have succeeded across the Top End of the Northern Territory because there are good supplies of food, water, and shelter. Pigs are omnivorous and are opportunistic feederseating plants that include crops, fruit, and vegetables and rooting extensively for tubers, worms, and soil invertebrates -and will exploit any temporarily abundant food. They also eat animal flesh, preying on small animals as well as scavenging on carrion [54]. Feral pigs are a significant food source for local Aboriginal people [51], mainly because of their abundance and availability. Some available radionuclide concentration data are summarised in Tables 4  and 5. Both datasets show the presence of high 210 Po concentrations and very high 210 Po/ 210 Pb ratios in the edible flesh.

Magpie Geese
Magpie geese (Anseranas semipalmata) are an important and popular dietary item in many Aboriginal communities in northern Australia and it has been estimated that up to 60% of Aboriginal people include magpie geese as a food source [53]. The average magpie goose can stand 70 cm tall and weigh 3 kg and during the late wet season and through the early dry season the eggs of magpie geese are consumed widely [51]. In their study Davy and Conway [26] found values for uranium and 226 Ra were higher for bones then in the flesh and liver of magpie geese. Koperski and Bywater [10] analysed flesh samples from magpie geese as part of a study of the impact of the Ranger mine, and found no significant difference between premining and mining period values. Tables 4 and 5 summarise some of the available activity concentration data [10,46]. In each case, the highest concentrations were obtained for 210 Po.

TERRESTRIAL FLORA
In the late wet and early dry seasons, vegetable foods become available and are harvested mainly by Aboriginal women. Altman [9] identified over 80 floral species used as bush foods. Although the contribution of vegetable bush foods to the Aboriginal diet has decreased in recent times due to the availability of market goods [51], these foods are still a significant potential radiological dose contributor. This is a potentially important pathway once a former minesite becomes available for public access after rehabilitation is finished.

Fruits
Early radiological studies were conducted by Davy and Conway [26]. They reported data for uranium and 226 Ra in native apples (Eugenia sp.) and native figs (Ficus henneana), and uranium in Pandanus palm fruit, from the ARR (Table 6). Koperski and Bywater [10] published results for premining and mining period analysis for red apples (Syzygium suborbiculare); see Table 7. They concluded that no statistical differences were found for the specific activities of the radionuclides analysed in foods sampled during premining and mining periods. , in a study on radionuclide uptake by plants on the Land Application (spray irrigation) Area of Ranger Uranium Mine, reported data for two fruit samples: Cocky Apple (Planchonia careya) and the Grey Plum (Persoonia falcata); see Table 8.

Root Vegetables
Martin et al. [46] reported activity concentrations, as well as CRs relative to total soil activity, for samples of cheeky yams (Dioscorea bulbifera) and Anbulubi roots (Eriosema chinense). The reported results are shown in Table 9. The differences between the results for the two species may be partly due to the fact that the yams were peeled whereas the anbulubi were not.

CONCLUSIONS
The research that has been undertaken into natural-series radionuclide uptake by edible flora and fauna of the Top End has mainly been conducted over the last 2 decades. As a result of the large number of possible radionuclide/food item combinations, many of the studies have concentrated on providing data suitable for calculation of CRs, although more detailed uptake studies have been undertaken for some species (freshwater mussels, turtles, and water lilies).
Despite the work that has been carried out to date, continuing study of radionuclide concentrations in Aboriginal bush foods of the region will be required for the foreseeable future, in order to provide Aboriginal people with the assurance that their food resources are being protected from mining operations. Some major areas requiring study are discussed below.
Firstly, an important factor in estimation of radiological dose is knowledge of the bushfood consumption by the relevant Aboriginal groups [9,56]. This includes knowledge of both the range and quantities of foods eaten, as well as of food preparation methods. Collection of this type of data on indigenous customary harvesting is a challenging task, particularly where quantitative data are required. This is because of the wide diversity of bush foods eaten, the fact that food collection tends to be opportunistic and often eaten at or close to the location that it is collected, and the considerable social changes occurring within the society (making the situation dynamic). As a result, it is unlikely that diet quantification will ever reach a level of reliability that is attainable for a non-Aboriginal society.
Secondly, there is relatively little available information on radionuclides in terrestrial animals and plants. Much of the available data, especially for terrestrial plants, are for concentrations in the edible portions rather than giving information on radionuclide uptake, and hence are of limited utility for predictive purposes. This information is very important for planning of uranium minesite rehabilitation, as after rehabilitation is finished the minesite may be accessed for collection of terrestrial food items. There are also few data available for bioaccumulation of radionuclides into certain other classes of Aboriginal foods, even for aquatic and semi-aquatic fauna (e.g., fats, eggs, liver, heart, bone marrow).
Finally, whereas the majority of studies to date have focussed on 226 Ra and/or uranium, these are not necessarily the only radionuclides of importance from a radiological impact point of view. Table 10 shows the percentage contribution by radionuclide to committed effective dose for a 10-year-old child from a release of water from either of two of the retention ponds at the Ranger mine (these predictions are based on calculations using CRs [57] and historical data for radionuclide concentrations in the retention pond waters; pond 4 is no longer in existence but is included here as an illustrative case). Although 226 Ra is the dominant contributor in the case of retention pond 2, in the case of pond 4 the predicted fraction of the dose due to 210 Po is significant. In each case, the relative contribution from uranium isotopes is low due to their low CRs in most aquatic foods and relatively low dose rate conversion factors for ingestion. In the case of the Ranger mine, protection against effects on the aquatic ecosystem rather than radiological effects on humans is the most limiting factor for releases of uranium [58]. According to present estimates, the total committed effective dose arising from water releases from the Ranger mine are extremely low (about 0.5 µSv/year for individuals living at Mudginberri billabong [57]). By comparison, the dose received due to the naturally occurring radionuclide concentrations is estimated to be 1.6 mSv/year for an adult and 2.2 mSv/year for a 10-year-old child (this estimate is based on the Aboriginal diet assumed in [59], ICRP dose conversion factors for ingestion [60], and measured concentration data from several of the studies discussed above).
For the natural (i.e., nonmining related) dose, the greatest percentage contributor is 210 Po, followed by 228 Ra and 226 Ra (final column of Table 10). The relatively high contribution from 210 Po is due to the high dose conversion factor for ingestion for this radionuclide, and to the high concentrations observed in faunal tissue. In particular, the measured concentrations of 210 Po were very high in liver, kidney, and intestine samples from buffalo and turtle, and in freshwater mussel and pig flesh. This has important consequences for the postrehabilitation scenario for the Ranger mine. In this situation, an important pathway for radiological dose will be erosion of waste rock material from the site. Unlike pond water releases, the uranium series radionuclides will be close to secular equilibrium in this material, and the relative contributions to dose by radionuclide are likely to be closer to the natural relative contributions (with the exception of 228 Ra) than to those for water release. Hence 210 Po is likely to be more important after rehabilitation than in the operational phase, and should be included in any future studies of radionuclide bioaccumulation in the region.