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Influence of macroalgal diversity on accumulation of radionuclides and heavy metals in Bulgarian Black Sea ecosystems
Journal of Environmental Radioactivity 100 (2009) 144–150
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Influence of macroalgal diversity on accumulation of radionuclides and heavy metals in Bulgarian Black Sea ecosystems Alexander Strezov*, Tzvetana Nonova Laboratory of Radiochemistry and Radiopharmacy, Institute for Nuclear Research and Nuclear Energy, Bulgarian Academy of Sciences, Blvd. Tzarigradsko shosse 72, 1784 Sofia, Bulgaria
a r t i c l e i n f o
a b s t r a c t
Article history: Received 8 March 2007 Received in revised form 15 August 2008 Accepted 18 September 2008 Available online 21 November 2008
Radionuclides and heavy metals were studied in green, brown and red Black Sea macroalgae by low-level gamma spectrometry and atomic absorption spectrometry. The samples were collected along the whole Bulgarian coast from 1996 to 2004. The levels have been depending on algae species, locations and year of sampling. The highest 137Cs levels were found in red Ceramium rubrum species from all studied locations, while 226Ra and 210Pb were up to three orders of magnitude higher in Bryopsis plumosa. The data showed that the red algae species (Rhodophyta) accumulate more heavy metals than the other phyla (except for Fe whose values were higher in green algae). The data confirmed that algae are valuable indicators of the environmental contamination. The observed elevated levels were mainly due to Danube, Dnieper and Dnester inputs in the NW corner of the Black Sea. Ó 2008 Published by Elsevier Ltd.
Keywords: Black Sea Macroalgae Radionuclides Trace metals Bioaccumulation
1. Introduction Radionuclides and metals are the major part of anthropogenic pollutants in the Black Sea marine ecosystems. The main sources of Black Sea pollution are atmospheric fallout, the big rivers (Danube, Dnieper, Dnester, etc.) that run-off in the northern part of the Black Sea as well as local pollutant emissions. Changes in the Black Sea radiation situation after the Chernobyl accident resulted in multiple studies of radionuclide accumulation processes in biota as the Black Sea received a great amount of radionuclide impact due to its geographical position. The increase of anthropogenic radionuclides in seawater caused changes in the background of the marine environment, in the water (Livingston et al., 1986; Nikitin et al., 1988; Keondjan et al., 1990; Polikarpov et al., 1991), suspended particles (Buesseler et al., 1987), sediment (Kulebakina and Polikarpov, 1989; Gulin et al., 2002) and biota. Heavy radionuclides affect the living organisms both as metals and as radiation sources, and they transfer as elements of the food chain (Aarkrog 1997). Trace metals play an important role in metabolism and both high or low concentrations can be harmful to biota. The main source of metals and radionuclide contamination of the Bulgarian
* Corresponding author. Tel.: þ359 27144637; fax: þ359 29753619. E-mail address: [email protected] (A. Strezov). 0265-931X/$ – see front matter Ó 2008 Published by Elsevier Ltd. doi:10.1016/j.jenvrad.2008.09.007
coast is local industry plus the input of big rivers – Danube, Dnieper, Dnester – in the north-west corner of the Black Sea. Since marine algae are well distributed along coasts and can be found in large quantities, many studies have been performed worldwide to characterize algae species for chemical, trace elements and radionuclide content (Calmet et al., 1991; Topcuoglu et al., 1996; Horn and Yan, 1998; Strezov et al., 1999; Christensen and Selnaes, 1999; Sartoni et al., 1999; Rissanen et al., 1999). The macrophytic species are among the most suitable bioindicators for nuclide and metal concentrations in marine ecosystems and play a major role in the trophic chain (Rainbow, 1995; Campanella et al., 2001; Cosma, 2002; Conti and Cecchetti, 2003). Green (Ulva sp., Enteromorpha sp., Chaetomorpha sp. and Cladophora sp.), Red (Ceramium sp. and Callithamnion sp.) and Brown (Cystoseira sp.) macroalgae are widespread in the littoral Black Sea ecosystems. They are adaptive towards the different condition changes of the habitat and can be found both in clean and contaminated regions. Many studies of environmental pollution have demonstrated the use of green (Ulva lactuca, Ulva rigida and Enteromorpha intestinalis) and red (Ceramium rubrum) algae species. Ulva and Enteromorpha species, both belonging to the Ulvaceae family, have been extensively used to monitor marine pollution in various geographical areas (Favero et al., 1996; Muse et al., 1999; Ho, 1990; Haritonidis and Malea, 1999). Ceramium sp. and Cystoseira sp. are among of the most studied red and brown algae and their ability to accumulate some radionuclides and metals are well known too.
A. Strezov, T. Nonova / Journal of Environmental Radioactivity 100 (2009) 144–150
145
Table 1 Sampling locations for green, brown and red macroalgae at Black Sea coast. Algae/location
Shabla
Green (Chlorophyta) algae Ulva rigida Cladophora vagabunda Enteromorpha intestinalis Chaetomorpha gracilis Bryopsis plumosa
þ þ þ þ
Brown (Phaeophyta) algae Cystoseira barbata Cystoseira crinita Red (Rhodophyta) algae Ceramium rubrum Corallina officinalis Callithamnion corymbosum
Rusalka
Kaliakra
Bjala
Ravda
þ þ þ þ
þ þ þ
þ
þ þ þ þ
þ þ
þ
þ
þ
þ
þ
Rossenetz
Maslen nos
Perla
Varvara
Ahtopol
Sinemoretz
Rezovo
þ þ
þ
þ
þ
þ þ
þ þ þ
þ þ þ þ þ
þ þ þ
þ þ
þ þ
þ þ
þ þ
þ þ
þ þ
þ
þ
þ
þ
þ
þ
þ
þ
Tuzlata
þ
þ þ
þ
þ
þ
þ
þ
þ
The main objective of this study was to determine radioactivity and metal levels in algae species distributed along the Bulgarian Black Sea coast during the period 1996–2004 and compare the accumulation capacity of different Bulgarian Black Sea macroalgae species. 2. Experimental Radionuclide and metal contents were determined in ten macroalgae species – five green, three red and two brown, sampled during the period 1992–2004. All plants were collected at 0.5–2 m depth from thirteen sites located along the whole Bulgarian Black Sea coast (Table 1, Fig. 1). Samples were washed with seawater, frozen and transported to the laboratory for analyses. Anthropogenic (137Cs) and natural (226Ra, 2I0Pb, 40K) radionuclides were determined by low-level gamma spectroscopy, using HPGe detector (Ortec type) with 35% counting efficiency and energy resolution 1.8 KeV (at 1332 KeV) in multilayer shielding. Trace metal content was determined using a Pye Unicam 1950 atomic absorption spectrophotometer with air-acetylene flame for Fe, Mn, Zn and Cu and by a Perkin–Elmer Zeeman 3030 spectrophotometer with graphite furnace for Cr, Pb and Cd. Quality assurance and accuracy were checked by means of a certified algae material NIES-CRM-3 (Chlorella sp.). The sample treatment, procedures, measurements, and precision of the analyses assessment are described elsewhere (Strezov et al., 1999; Strezov and Nonova, 2003; Nonova and Strezov, 2005).
3. Results and discussion 3.1. Radionuclides The measured activity concentrations for anthropogenic (137Cs) and natural (226Ra, 210Pb and 40K) radionuclides in algae (mean SD, range in Bq/kg dry wgt) are presented in Table 2. Cesium-137 is one of the most frequently studied nuclides entered the Black Sea region due to the global fallout and Chernobyl accident. This nuclide enters marine algae metabolism because it is a chemical analogue of K and Na. Red macrophytes (Rhodophyta, mainly C. rubrum) accumulated 137 Cs to a higher extent compared to the other two – brown Phaeophyta and green Chlorophyta phyla (Al-Masri, 2002; Topcuoglu et al., 1996). Cesium-137 varied not only between different algae species, but also within the same species from different sites. This fact is due to the impact of several (abiotic, biological anthropogenic) factors as well as the inhomogeneous distribution of Cs in the ecosystems (Buesseler et al., 1987). The mean 137Cs values obtained in red Black Sea algae were higher than those for brown and green algae. Topcuoglu et al. (1996) and Topcuoglu and Gungor (1999) reported similar values (3.8–9.8 Bq/kg) for the same green, red and brown algae species in the Black Sea. The 137Cs content measured by Romanian authors Dovlete and Osvath (1992) and Bologa et al. (1998, 1999) was in the range 2–18 Bq/kg, close to those obtained by us.
þ þ þ
þ
Data were obtained for 40K concentrations – the highest values were for Chaetomorpha gracilis and Callithamnion corymbosum species. Similar levels were measured in green Cladophora sp., brown Cystoseira sp. and red Ceramium sp. Natural 40K is a chemical analogue of radiocesium and the existence of correlation between 40K and 137Cs is interesting as the origin of the nuclides is different. The comparative assessment of results was performed in all locations. The correlation coefficient for C. rubrum r ¼ 0.597 is significant at p < 0.001, N ¼ 26. The positive correlation between 40K and 137Cs in studied red macrophytes shows that these elements follow a similar transfer pattern. All alga samples were analyzed by gamma spectrometry for natural radionuclide contents from 238U series (226Ra, 210Pb) and 40 K, given also in Table 2. Accumulation intervals for 226Ra were close for the two brown and for green U. rigida, Cladophora vagabunda and E. intestinalis as well. The 226Ra mean values in different species can be arranged: C. rubrum > C. vagabunda w Cystoseira barbata > Cystoseira crinita w U. rigida w E. intestinalis > C. gracilis > C. corymbosum w Corallina officinalis. Data for the 210Pb mean values in all red, green and brown algae can be arranged depending on algae species in the following order: C. rubrum > C. corymbosum > C. officinalis w C. crinita > C. gracilis > E. intestinalis > C. barbata > C. vagabunda > U. rigida. Generally, red algae accumulated natural nuclides to higher concentrations, while there is no clear colour dependence of 210Pb accumulation in the other alga phyla. The measured nuclide content in Black Sea algae can be used also as a characterization of radionuclide level at different Bulgarian Black Sea coastal regions. The results for 226Ra and 210Pb algae are indicators for Ra and Pb quantities in seawater and sediments. These data can be used for comparison of the different geographical regions of the Bulgarian Black Sea shore from north to south (presented in Fig. 2). Judging from the 226Ra content (9– 39 Bq/kg) in the red alga C. rubrum, the studied locations can be arranged: Rusalka < Bjala < Maslen nos < Perla < Ahtopol < Sinemoretz < Shabla < Rezovo < Varvara < Ravda < Kaliakra < Tuzlata. The 210Pb concentrations in C. rubrum from all samples were in the range 4–41 Bq/kg. It should be noted that 210Pb content was higher than its parent 226Ra in Ravda, Maslen nos, Ahtopol and Rezovo (highest in Ravda) probably due to fresh sediment deposits carried by the seawater currents. The data show that red algae selectively accumulated 210Pb and 226 Ra to a measurable extent from U series. Al-Masri (2002) reports also that red algae in the Mediterranean accumulate 210Pb and radium isotopes to higher levels and this is an indication for their affinity towards these isotopes.
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A. Strezov, T. Nonova / Journal of Environmental Radioactivity 100 (2009) 144–150
ROMANIA
N Shabla Rusalka Tuzlata
Kaliakra
Varna Bjala
BLACK SEA
Ravda
Burgas
Rossenetz Maslen Nos Perla Varvara Ahtopol Sinemoretz Rezovo
TURKEY
Fig. 1. Sampling locations along the Bulgarian Black Sea coast.
Higher natural nuclide values were measured at Rossenetz (226Ra – 118 Bq/kg and 210Pb – 190 Bq/kg) where high values were measured at the beach and in the bay sediments (137Cs content is also higher 34 Bq/kg). This site is known for the high content of natural nuclides which are a by-product of the exploitation of a copper mine in the vicinity. The effect of phosphate ore unloading operations may be the cause of higher 226Ra and 210Pb values in the beaches, sediments and biota from Shabla, Tuzlata and Kaliakra sites (Varna bay) and Ravda (Burgas bay), but local mineral contribution should not be neglected. A recent study supported by IAEA was performed to assess the impact of unloading cargoes of phosphate ore from ships,
showing the impact on the near marine environment at the Mediterranean sea coast (Al-Masri, 2002). Such activities are performed also at Bulgarian seaports and, together with mining activities in some places, led to a higher natural nuclide content at the beaches, in sea sediments and biota. Data were obtained in some of the studied algae species for 232 Th series nuclides – 228Ac, 208Tl. The concentrations of the nuclides were low, varying between 1 and 7 Bq/kg for 228Ac and 1 and 3 Bq/kg for 208Tl. The 228Th concentrations were close to the lower limit of detection (LLD) level (same as 234Th), meaning that daughters of 238U are more readily accumulated compared to 232Th.
A. Strezov, T. Nonova / Journal of Environmental Radioactivity 100 (2009) 144–150
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Table 2 Radionuclide accumulation in green, brown and red Black Sea macroalgae (in Bq/kg dry wgt; N – number of samples). Algae
137
226
Cs
N
210
Ra
40
Pb
K
Mean SD
Range
Mean SD
Range
Mean SD
Range
Mean SD
Range
Green algae Ulva rigida Enteromorpha intestinalis Cladophora vagabunda Chaetomorpha gracilis Bryopsis plumosa
14 9 11 5 5
4.1 0.7 3.3 0.8 4.0 0.8 2.3 0.8 2.1 0.6
1.5–10 1.4–7 2.0–9 1.2–5.3 1.4–4.1
81 82 12 2 72 900 120
3–16 3–15 4–18 4–11 650–1300
61 10 2 81 11 2 63 18
3–15 3–15 3–14 5–16 45–100
596 62 690 60 1300 180 1860 200 740 90
460–985 370–1230 520–2330 1220–2500 570–870
Brown algae Cystoseira barbata Cystoseira crinita
18 21
6.1 0.5 5.3 0.4
3–10 2.6–10
12 2 81
3–17 2–17
91 12 1
3–18 2–21
1350 190 1530 90
130–1980 1340–1990
Red algae Ceramium rubrum Callithamnion corymbosum Corallina officinalis
23 6 8
9.7 0.8 4.4 0.7 2.4 0.5
4–18 2.9–6.5 1.2–5.4
21 2 62 61
9–39 3–17 2–11
16 2 13 4 12 2
4–41 4–30 4–22
1343 98 1580 110 140 10
860–2100 1230–1920 124–170
The highest measured natural nuclide concentrations were determined in the green alga Bryopsis plumosa (Table 2, Fig. 3). This is one of the widespread Black Sea green macrophytes and it differs from the other algae because of its life cycle and maximum of development in winter. This green alga seems to extract some of 238 U daughters – 226Ra, 210Pb and 232Th daughters – 228Ra, 228Ac, 208 Tl, 212Bi, 212Pb from the seawater up to 1000–2000 Bq/kg level that is approximately three orders of magnitude higher than all other alga species collected from the same site. Dovlete (1990), tras¸cu (1995) also report the high Dovlete and Osvath (1992) and Pa natural radionuclide content in the green B. plumosa. Variations of 137Cs, 226Ra, 210Pb concentration depending on sampling year for C. rubrum from all sampling sites are presented in Fig. 4. The observed 137Cs, 226Ra and 210Pb concentrations have been almost constant (except 2001–2002). 3.2. Metals The mean values for Fe varied in the range 80–3530 mg/kg, the highest measured mean content was 1500 mg/kg in green Cladophora sp. Manganese ranged 7–350 mg/kg – with the highest, 180 mg/kg, in Chaetomorpha sp. (Table 3). The element Cu is one of the most biologically important metals and its compounds usually exist in the biosphere only in trace quantities, participating in the biological circle. Increase of Cu content may lead to a substantial damage in living organisms. The Cu concentration variations were in the range of 1–18 mg/kg for green and brown algae while for the red species the range was 3– 26 mg/kg. These data are close to the range obtained by other authors (Campanella et al., 2001; Topcuog˘lu et al., 2001) for
Fig. 2. Mean
226
Ra and
210
Pb content in Ceramium rubrum.
analogous algae species from neighboring seas (Mediterranean, Marmara, etc.) with exception of C. officinalis (8.5–26.4 mg/kg). The data for Zn, Cr, Pb and Cd were in the range 7–48 mg/kg, 0.5–24.6 mg/kg, 0.6–7.6 mg/kg and 0.2–2.9 mg/kg, respectively. Zinc forms different inorganic and organic complexes in seawater and about 50% of Zn is in the form of free ion in surface waters (Bruland, 1983). Sulphide forms of Zn prevail in greater depths of the Black Sea sediments (Landing and Lewis, 1991). The metals Cr, Cd and Pb are among the major hazardous contaminants in ecosystems – Cr is in the form of complexes bound by metalo-enzymes, leading to its accumulation by biota in high concentrations. Cadmium is toxic and poisonous for living organisms even in low concentrations. The behavior of Pb in water is complex and it is found in seawaters mainly in the form of different organic compounds. The results (histogram of mean values, data range) for trace metals in the three macrophytic phyla are compared in Fig. 5. All macroalgae species accumulated Cd, Cu, Pb and Zn to a similar extent, while the red and green algae have similarity in Cr and Mn content. The data show that the red algae species (Rhodophyta) accumulate metals higher than the other phyla (except Fe whose values are higher in green algae because of the chlorophyll). All data for the whole Bulgarian coast (about 300 km long) obtained from 13 sampling sites distributed from northern border to southern are evaluated by multivariable cluster analysis – Ward’s method (STATISTICA for Windows, StatSoft Inc., 1998, www.statsoft. com). Cluster analysis for the red C. rubrum data is presented because this alga is abundant along the whole Bulgarian Black Sea coast and accumulates metals to considerable concentrations. The results of the statistical analysis led to grouping in three clusters of all 12 Ceramium sp. sampling locations, depending on 4 radionuclides and 7 metals (about 80 samples) for the whole 1996–2004 period (Fig. 6a). In the first cluster are the locations with the highest measured 137Cs, 226Ra and 40K concentrations – Maslen nos, Perla, Kaliakra and Tuzlata. These sites are divided in two subgroups (Maslen nos, Perla and Kaliakra, Tuzlata), whose grouping is clear because of geographical proximity and similarity in the sediments matrix – slime. The southern sites Ahtopol, Varvara and Sinemoretz (þcentral Ravda) comprise the second cluster having lower nuclide concentrations than the first cluster (here also similarity in the sediment matrix – sand). The third cluster with the lowest concentrations – Shabla, Sinemoretz, Rusalka and Bjala also connects sites with sand matrix which sorbes nuclides to the lowest level. Mean nuclide values in the determined clusters are presented in Table 4. Second cluster contains sites with highest mean 210Pb concentrations (mainly in the south) which is in conformity with the presence of metal mines from antiquity in the region.
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2200
Ra-226
2000
Pb-210
Bryopsis plumosa Mean; Whisker: Min, Max
Ac-228
1800
Ra-224 1600
Tl-208
Bq/kg
1400 1200 1000 800 600 400 200 0
Ahtopol 1996
Shabla 1999
Shabla 1998
Rusalka 2003
Shabla 2003
Fig. 3. Radionuclide content in green algae Bryopsis plumosa.
60 55 50 45
Cs-137
Mean; Whisker: Min, Max
Ra-226 Pb-210
40
Bq/kg
35 30 25 20 15 10 5 0
1996
1998
1999
2000
2001
2002
2003
2004
Fig. 4. Radionuclide content in macrophytes for different sampling years.
Table 3 Trace metals in macroalgae species (mean SD (range in parentheses) in mg/kg). Element (mg/kg)
Chlorophyta Ulva rigida
Enteromorpha intestinalis
Cladophora vagabunda
Chaetomorpha gracilis
Bryopsis plumosa
Cystoseira barbata
Cystoseira crinita
Ceramium rubrum
Callithamnion corymbosum
Corallina officinalis
Cd
0.8 0.2 (0.3–2.1) 1.8 0.4 (0.5–3.2) 5.6 0.9 (2.2–10.9) 430 90 (110–1000) 35 8 (9–108) 1.6 0.1 (1.2–1.8) 16 3 (7–32)
0.8 0.2 (0.3–1.6) 5.3 0.9 (1.9–8.6) 71 (1.3–10.5) 1010 80 (190–1940) 47 8 (21–71) 2.4 0.2 (1.7–3.2) 14 1 (10–17)
1.0 0.3 (0.3–2.9) 71 (1.8–25) 61 (4–16) 1500 310 (810–3530) 170 20 (38–350) 3.5 0.7 (1.7–7.5) 19 4 (8–48)
1.3 0.3 (0.5–2.9) 71 (2–14) 51 (2–9) 520 80 (160–880) 180 20 (100–230) 2.7 0.3 (1.2–4.6) 12 2 (6–18)
0.40 0.06 (0.25–0.42) 71 (4–10) 81 (1–18) 340 30 (310–400) 60 10 (26–94) 3.8 0.6 (1.7–7.6) 19 4 (9.4–31)
0.32 0.03 (0.20–0.43) 2.3 0.6 (0.7–5.7) 51 (1.4–9.2) 440 90 (120–790) 47 9 (7–86) 1.4 0.2 (0.6–2.1) 17 2 (8–26)
0.44 0.06 (0.24–0.75) 3.9 0.7 (1.3–6.5) 72 (3.8–17) 260 60 (80–450) 32 9 (11–97) 1.7 0.2 (1.2–2.4) 20 3 (12–33)
0.8 0.1 (0.3–1.3) 6.1 1.4 (0.8–16.5) 7.6 0.8 (3.4–12.2) 850 150 (140–1890) 121 22 (30–320) 2.2 0.3 (1.3–3.8) 22 3 (7–39)
0.53 0.20 (0.2–1.2) 3.7 0.6 (1.6–5.6) 5.4 0.9 (2.8–8.5) 880 70 (290–1850) 87 15 (33–200) 2.3 0.4 (1.4–3.6) 18 3 (11–25)
0.73 0.24 (0.4–1.2) 4.8 0.3 (1.3–10.8) 15 2 (8.5–26) 600 40 (280–800) 55 9 (35–88) 1.4 0.1 (1.3–1.5) 13 2 (10–15)
Cr Cu Fe Mn Pb Zn
Phaeophyta
Rhodophyta
A. Strezov, T. Nonova / Journal of Environmental Radioactivity 100 (2009) 144–150
70
400 350
Cu
60
300
Mn
50
250
Zn
Cd Cr Pb Rb
40
mg/kg
mg/kg
149
200 150
Zr 30 20
100 10
50 0
0
-50
-10
Rhodophyta
Phaeophyta
Chlorophyta
Chlorophyta
Rhodophyta
Phaeophyta
Fig. 5. Mean content of trace metals in algae phyla.
Tree Diagram for 12 Cases Ward`s method, Euclidean distances
Tree Diagram for 12 Cases Ward`s method, Euclidean distances Shabla Sinemoretz Rusalka Bjala Ravda Ahtopol Varvara Rezovo Tuzlata Kaliakra Maslen nos Perla
Shabla Sinemoretz Rusalka Rezovo Bjala Ravda Ahtopol Maslen nos Varvara Tuzlata Kaliakra Perla
radionuclides
0
1
2
3
4
5
6
7
metals
1
2
3
4
5
6
7
8
Linkage Distance
Linkage Distance Fig. 6. Cluster analysis of contaminants in Ceramium rubrum.
There is a resemblance between the cluster diagrams of nuclides and metals because nuclides are also trace metal contaminants that both have an impact on biota in marine ecosystems. The grouping of locations shows logical geographic dependence of contaminant content together with separation of clean areas. The tree diagram for metals in C. rubrum contains two major clusters. The first (as for nuclides) contains geographically close sites Kaliakra, Tuzlata plus Perla with higher content. The second cluster is divided in two subparts whose variation values are close. The lower metal content is in Shabla, Rusalka, Bjala, Sinemoretz and Rezovo which are situated in the far north and south parts of the Black Sea coast. Mean metal values in C. rubrum obtained for the different clusters are given in Table 5.
4. Conclusions Radionuclide and metal accumulation capacity has been studied in three algae phyla along the Bulgarian Black Sea coast during the period 1996–2004. The red alga C. rubrum had the highest 137Cs
Table 4 Mean nuclide values, obtained for Ceramium rubrum by clusters [Bq/kg]. Nuclide
Cluster I [(Maslen nos, Perla) þ (Kaliakra, Tuzlata)]
Cluster II {[(Ahtopol, Varvara) þ Rezovo] þ Ravda}
Cluster III [(Shabla, Sinemoretz) þ (Rusalka, Blala)]
137
12.6 21 14 1639
7.9 17 20 1104
7.6 14 6 1285
Cs Ra Pb 40 K 226 210
levels. The green B. plumosa accumulated natural radionuclides by three orders of magnitude higher than other algae sampled from the same locations. B. plumosa is one of the widespread Black Sea macrophytes and differs from the other studied algae by the life cycle (winter) and maximum of development. This alga seems to extract preferably some of 238U daughters – 226Ra, 210Pb and 232Th daughters 228Ra, 228Ac, 208Tl. The data show that there is no serious contamination of the Bulgarian coast with radionuclides, as no nuclear activities have been carried out in the region. Elevated natural nuclide levels were mostly due to mining of phosphate ores and minerals, carried out in the vicinity of sampling sites. The status of the marine environment in all studied areas was evaluated by cluster analysis of macroalgae data from all geographic zones. Results showed a geographical distribution of contaminants in tree diagrams for radionuclides and metals. The elevated levels were mainly due to Danube, Dnieper and Dnester Table 5 Mean metal values, obtained for Ceramium rubrum by clusters [mg/kg]. Element Cluster I Cluster II.1 Cluster II.2 [(Tuzlata, Kaliakra) {[(Ahtopol, Ravda) {[(Sinemoretz, Rusalka) þ Perla] þ Maslen nos] þ Varvara} þ Shabla] þ Rezovo} þ Bjala Cd Cr Cu Fe Mn Pb Rb Sr Zn
1.06 9.6 10.7 1490 443 2.9 11 206 34
0.57 3.9 9.3 565 92 1.6 10 155 25
1.04 5.7 4.4 681 128 2.2 13 128 15
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input in the NW corner of the Black Sea, as well as due to a pollution of regional centers Varna and Burgas. The presented data on radionuclides and metals in macroalgae will be used as a baseline for further investigations of contamination of marine ecosystems along the Bulgarian Black Sea coast. References Aarkrog, A., 1997. Radioactivity in the oceans. Journal of Radiological Protection 17, 210–213. Al-Masri, M.S., 2002. Marine environment studies on the Syrian Coast: biomonitors. In: Proceeding of CIESM Workshop – Mediterranean Mussel Watch, 18–20 April 2002, Marseille, France, pp. 3–6. Bologa, A.S., Apas, M., Cociasu, A., Cuingioglu, E., Patrascu, V., Pecheanu, I., Piescu, V., Popa, L., 1999. Present level of contaminants in the Romanian Black Sea sector. IAEA-TECDOC-1094, pp. 58–63. Bologa, A.S., Patrascu, V., Cuingioglum, E., 1998. Distribution of total beta radioactivity, Sr-90 and Cs-137 content in the Romanian and NW Black Sea 1994–1995. Raport Comm. International de Mer Mediteranee. 35, 234–235. Bruland, K.W., 1983. Trace elements in seawater. In: Riley, Chester (Eds.), Chemical Oceanography, vol. 8. Academic Press, London, pp. 157–220. Buesseler, K.O., Livingston, H.D., Hohjo, S., Hay, B.J., Manganini, S.J., Degens, E., Ittekot, V., Izdar, E., Konuk, T., 1987. Chernobyl radionuclides in a Black Sea sediment trap. Nature 329, 825–828. Calmet, S., Charmasson, G., Gontier, A., Meinesz, C.F., 1991. Chernobyl radionuclides in the Mediterranean seagrass Posidonia oceanica. Journal of Environmental Radioactivity 13, 157–173. Campanella, L., Conti, M.E., Cubadda, F., Sucapane, C., 2001. Trace metals in seagrass, algae and molluscs from an uncontaminated area in the Mediterranean. Environmental Pollution 111, 117–126. Conti, M.E., Cecchetti, G., 2003. A biomonitoring study: trace metals in algae and molluscs from Tyrrhenian coastal areas. Environmental Research 93, 99–112. Cosma, C., 2002. Some aspects of radioactive contamination after Chernobyl accident in Romania. Journal of Radioanalytical and Nuclear Chemistry 251 (2), 221–226. Christensen, G.C., Selnaes, T.D., 1999. Study of marine activity along the Norwegian coast, 1980–1984. In: Marine Pollution, vol. 49. International Atomic Energy Agency (IAEA-TECDOC-1094, IAEA-SM-339). Dovlete, C., Osvath, I., 1992. Radium and its daughters in Bryopsis plumosa. Radiation Protection Dosimetry 45, 301–302. Dovlete, C., 1990. Radium and its daughters in Bryopsis plumosa. Rapp. Commun. Int. Mer. Medit. 32 (1), 232. Favero, N., Cattalini, F., Bertaggia, D., Albergoni, V., 1996. Metal Accumulation in Biological Indicator (Ulva rigida) from the lagoon of Venice (Itaki). Archives of Environmental Contamination and Toxicology 31 (1), 9–18. Gulin, S.B., Polikarpov, G.G., Egorov, V.N., Martin, J.M., Korotkov, A.A., Stokozov, N.A., 2002. Radioactive contamination of the north-western Black Sea sediments. Estuarine, Coastal and Shelf Science 54, 541–549. Haritonidis, S., Malea, P., 1999. Bioaccumulation of Metals by the Green Alga Ulva Rigida from Thermaikos Gulf, Greece. Environmental Pollution 104, 365–372.
Horn, X., Yan, X., 1998. Study on the concentration and seasonal variation of inorganic elements in 35 species of marine algae. The Science of the Total Environment 222, 141–156. Ho, Y., 1990. Ulva lactuca as bioindicator of metal contamination in intertidal waters in Hong Kong. Hydrobiology 203, 73–81. Keondjan, V.P., Kudin, A.M., Terehin, Yu., 1990. Practical Ecology of Sea Regions. The Black Sea. Naukova Dumka, Kiev, pp. 46–56. Kulebakina, L., Polikarpov, G., 1989. Radiological investigation of Black Sea ecosystems after the Chernobyl accident. In: Proceedings of the Conference on Radioecology High Tatras, Czechoslovakia, pp. 131–155. Landing, W.M., Lewis, B.L., 1991. Thermodynamic modeling of trace metal speciation in the Black Sea. In: Izdar, E., Murray, J.W. (Eds.), Black Sea Oceanography, pp.125–160. Livingston, H.D., Buesseler, K.O., Izdar, E., Konik, T., 1986. Characteristics of Chernobyl Fallout in the Southern Black Sea. EML-460. US Department of Energy, Environmental Measurement Laboratory, New York, pp. 214–223. Muse, J.O., Stripeikis, J.D., Fernandez, F.M., Huicqui, L., Tudino, M., Carducci, C., Troccoli, O., 1999. Seaweeds in the assessment of heavy metal pollution in the Gulf San Jorge, Argentina. Environmental Pollution 104, 315–322. Nikitin, A.I., Medinets, W.I., Tchumishew, W., Katrich, I., Wakulowskij, S.M., Kozlow, A.I., Lepeshkin, W.I., 1988. Radioaktiwnoe zagryazenie Chernogo morya wsledstwie awarii na Chernobilskoj AEC po sostoyaniu na oktyabr 1986. Atomnaya Energiya 6 (2), 134–136. Nonova, Tz, Strezov, A., 2005. Radionuclide uptake in red macroalgae from the Bulgarian Black Sea coast. Journal of Radioanalytical and Nuclear Chemistry 266 (3), 411–417. ¨ zhan, E. tras¸cu, V., 1995. Relative content of radionuclides in aquatic components. In: O Pa (Ed.), Proceedings of the Second International Conference on the Mediterranean Coastal Environment, Tarragona Spain, October (1995). Polikarpov, G.G., Kulebakina, L.G., Timoshchuk, V.I., Stokozov, N.A., 1991. 90Sr and 137 Cs in surface waters of the Dnieper River, the Black Sea and the Aegean Sea in 1987 and 1988. Journal of Environmental Radioactivity 13, 25–34. Rainbow, P., 1995. Biomonitoring of heavy metal availability in the marine environment. Marine Pollution Bulletin 31, 183–192. Rissanen, K., Ikaheimonen, T.K., Matishov, D.G., Matishov, G.G., 1999. Radioactive cesium, cobalt, and plutonium in biota, algae, and sediment in the unrestricted areas of the Russian Arctic Sea. In: Marine Pollution, vol. 12. International Atomic Energy Agency (IAEA-TECDOC-1094, IAEA-SM-354). Sartoni, G., De Biasi, A.M., Cryptogami, E., 1999. A survey of the marine algae of Milos Hand Greece. Algol 20, 271–283. Strezov, A.S., Nonova, Tz.P., 2003. Radionuclide and heavy metal content in sediments and macrophytes from Black Sea ecosystems. Ecology 2, 238–249. Strezov, A.S., Stoilova, T., Jordanova, A.V., Ayranov, M., Petkov, N., 1999. Determination of caesium and natural radionuclide concentrations in sediments, algae and water. Water Science and Technology 39, 21–26. Topcuog˘lu, S., Gu¨ven, K.C., Kirbasoglu, C., Gu¨ngo¨r, N., Yilmaz, Y.Z., 2001. Heavy metals in marine algae from Sile in the Black Sea, 1994–1997. Bulletin of Environmental Contamination and Toxicology 67, 288–294. Topcuoglu, S., Gungor, N., 1999. Radionuclide concentrations in macroalgae and sediment samples from the Bosphorus. Turkish Journal of Marine Sciences 5, 19. Topcuoglu, S., Gu¨ven, K.C., Ku¨cu¨kcezzar, R., Kut, D., Esen, N., 1996. The natural depuration of 137Cs radionuclide in the Black Sea macroalgae. Journal of Radioanalytical and Nuclear Chemistry 214, 319–325.
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Influence of macroalgal diversity on accumulation of radionuclides and heavy metals in Bulgarian Black Sea ecosystems Alexander Strezov*, Tzvetana Nonova Laboratory of Radiochemistry and Radiopharmacy, Institute for Nuclear Research and Nuclear Energy, Bulgarian Academy of Sciences, Blvd. Tzarigradsko shosse 72, 1784 Sofia, Bulgaria
a r t i c l e i n f o
a b s t r a c t
Article history: Received 8 March 2007 Received in revised form 15 August 2008 Accepted 18 September 2008 Available online 21 November 2008
Radionuclides and heavy metals were studied in green, brown and red Black Sea macroalgae by low-level gamma spectrometry and atomic absorption spectrometry. The samples were collected along the whole Bulgarian coast from 1996 to 2004. The levels have been depending on algae species, locations and year of sampling. The highest 137Cs levels were found in red Ceramium rubrum species from all studied locations, while 226Ra and 210Pb were up to three orders of magnitude higher in Bryopsis plumosa. The data showed that the red algae species (Rhodophyta) accumulate more heavy metals than the other phyla (except for Fe whose values were higher in green algae). The data confirmed that algae are valuable indicators of the environmental contamination. The observed elevated levels were mainly due to Danube, Dnieper and Dnester inputs in the NW corner of the Black Sea. Ó 2008 Published by Elsevier Ltd.
Keywords: Black Sea Macroalgae Radionuclides Trace metals Bioaccumulation
1. Introduction Radionuclides and metals are the major part of anthropogenic pollutants in the Black Sea marine ecosystems. The main sources of Black Sea pollution are atmospheric fallout, the big rivers (Danube, Dnieper, Dnester, etc.) that run-off in the northern part of the Black Sea as well as local pollutant emissions. Changes in the Black Sea radiation situation after the Chernobyl accident resulted in multiple studies of radionuclide accumulation processes in biota as the Black Sea received a great amount of radionuclide impact due to its geographical position. The increase of anthropogenic radionuclides in seawater caused changes in the background of the marine environment, in the water (Livingston et al., 1986; Nikitin et al., 1988; Keondjan et al., 1990; Polikarpov et al., 1991), suspended particles (Buesseler et al., 1987), sediment (Kulebakina and Polikarpov, 1989; Gulin et al., 2002) and biota. Heavy radionuclides affect the living organisms both as metals and as radiation sources, and they transfer as elements of the food chain (Aarkrog 1997). Trace metals play an important role in metabolism and both high or low concentrations can be harmful to biota. The main source of metals and radionuclide contamination of the Bulgarian
* Corresponding author. Tel.: þ359 27144637; fax: þ359 29753619. E-mail address: [email protected] (A. Strezov). 0265-931X/$ – see front matter Ó 2008 Published by Elsevier Ltd. doi:10.1016/j.jenvrad.2008.09.007
coast is local industry plus the input of big rivers – Danube, Dnieper, Dnester – in the north-west corner of the Black Sea. Since marine algae are well distributed along coasts and can be found in large quantities, many studies have been performed worldwide to characterize algae species for chemical, trace elements and radionuclide content (Calmet et al., 1991; Topcuoglu et al., 1996; Horn and Yan, 1998; Strezov et al., 1999; Christensen and Selnaes, 1999; Sartoni et al., 1999; Rissanen et al., 1999). The macrophytic species are among the most suitable bioindicators for nuclide and metal concentrations in marine ecosystems and play a major role in the trophic chain (Rainbow, 1995; Campanella et al., 2001; Cosma, 2002; Conti and Cecchetti, 2003). Green (Ulva sp., Enteromorpha sp., Chaetomorpha sp. and Cladophora sp.), Red (Ceramium sp. and Callithamnion sp.) and Brown (Cystoseira sp.) macroalgae are widespread in the littoral Black Sea ecosystems. They are adaptive towards the different condition changes of the habitat and can be found both in clean and contaminated regions. Many studies of environmental pollution have demonstrated the use of green (Ulva lactuca, Ulva rigida and Enteromorpha intestinalis) and red (Ceramium rubrum) algae species. Ulva and Enteromorpha species, both belonging to the Ulvaceae family, have been extensively used to monitor marine pollution in various geographical areas (Favero et al., 1996; Muse et al., 1999; Ho, 1990; Haritonidis and Malea, 1999). Ceramium sp. and Cystoseira sp. are among of the most studied red and brown algae and their ability to accumulate some radionuclides and metals are well known too.
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145
Table 1 Sampling locations for green, brown and red macroalgae at Black Sea coast. Algae/location
Shabla
Green (Chlorophyta) algae Ulva rigida Cladophora vagabunda Enteromorpha intestinalis Chaetomorpha gracilis Bryopsis plumosa
þ þ þ þ
Brown (Phaeophyta) algae Cystoseira barbata Cystoseira crinita Red (Rhodophyta) algae Ceramium rubrum Corallina officinalis Callithamnion corymbosum
Rusalka
Kaliakra
Bjala
Ravda
þ þ þ þ
þ þ þ
þ
þ þ þ þ
þ þ
þ
þ
þ
þ
þ
Rossenetz
Maslen nos
Perla
Varvara
Ahtopol
Sinemoretz
Rezovo
þ þ
þ
þ
þ
þ þ
þ þ þ
þ þ þ þ þ
þ þ þ
þ þ
þ þ
þ þ
þ þ
þ þ
þ þ
þ
þ
þ
þ
þ
þ
þ
þ
Tuzlata
þ
þ þ
þ
þ
þ
þ
þ
þ
The main objective of this study was to determine radioactivity and metal levels in algae species distributed along the Bulgarian Black Sea coast during the period 1996–2004 and compare the accumulation capacity of different Bulgarian Black Sea macroalgae species. 2. Experimental Radionuclide and metal contents were determined in ten macroalgae species – five green, three red and two brown, sampled during the period 1992–2004. All plants were collected at 0.5–2 m depth from thirteen sites located along the whole Bulgarian Black Sea coast (Table 1, Fig. 1). Samples were washed with seawater, frozen and transported to the laboratory for analyses. Anthropogenic (137Cs) and natural (226Ra, 2I0Pb, 40K) radionuclides were determined by low-level gamma spectroscopy, using HPGe detector (Ortec type) with 35% counting efficiency and energy resolution 1.8 KeV (at 1332 KeV) in multilayer shielding. Trace metal content was determined using a Pye Unicam 1950 atomic absorption spectrophotometer with air-acetylene flame for Fe, Mn, Zn and Cu and by a Perkin–Elmer Zeeman 3030 spectrophotometer with graphite furnace for Cr, Pb and Cd. Quality assurance and accuracy were checked by means of a certified algae material NIES-CRM-3 (Chlorella sp.). The sample treatment, procedures, measurements, and precision of the analyses assessment are described elsewhere (Strezov et al., 1999; Strezov and Nonova, 2003; Nonova and Strezov, 2005).
3. Results and discussion 3.1. Radionuclides The measured activity concentrations for anthropogenic (137Cs) and natural (226Ra, 210Pb and 40K) radionuclides in algae (mean SD, range in Bq/kg dry wgt) are presented in Table 2. Cesium-137 is one of the most frequently studied nuclides entered the Black Sea region due to the global fallout and Chernobyl accident. This nuclide enters marine algae metabolism because it is a chemical analogue of K and Na. Red macrophytes (Rhodophyta, mainly C. rubrum) accumulated 137 Cs to a higher extent compared to the other two – brown Phaeophyta and green Chlorophyta phyla (Al-Masri, 2002; Topcuoglu et al., 1996). Cesium-137 varied not only between different algae species, but also within the same species from different sites. This fact is due to the impact of several (abiotic, biological anthropogenic) factors as well as the inhomogeneous distribution of Cs in the ecosystems (Buesseler et al., 1987). The mean 137Cs values obtained in red Black Sea algae were higher than those for brown and green algae. Topcuoglu et al. (1996) and Topcuoglu and Gungor (1999) reported similar values (3.8–9.8 Bq/kg) for the same green, red and brown algae species in the Black Sea. The 137Cs content measured by Romanian authors Dovlete and Osvath (1992) and Bologa et al. (1998, 1999) was in the range 2–18 Bq/kg, close to those obtained by us.
þ þ þ
þ
Data were obtained for 40K concentrations – the highest values were for Chaetomorpha gracilis and Callithamnion corymbosum species. Similar levels were measured in green Cladophora sp., brown Cystoseira sp. and red Ceramium sp. Natural 40K is a chemical analogue of radiocesium and the existence of correlation between 40K and 137Cs is interesting as the origin of the nuclides is different. The comparative assessment of results was performed in all locations. The correlation coefficient for C. rubrum r ¼ 0.597 is significant at p < 0.001, N ¼ 26. The positive correlation between 40K and 137Cs in studied red macrophytes shows that these elements follow a similar transfer pattern. All alga samples were analyzed by gamma spectrometry for natural radionuclide contents from 238U series (226Ra, 210Pb) and 40 K, given also in Table 2. Accumulation intervals for 226Ra were close for the two brown and for green U. rigida, Cladophora vagabunda and E. intestinalis as well. The 226Ra mean values in different species can be arranged: C. rubrum > C. vagabunda w Cystoseira barbata > Cystoseira crinita w U. rigida w E. intestinalis > C. gracilis > C. corymbosum w Corallina officinalis. Data for the 210Pb mean values in all red, green and brown algae can be arranged depending on algae species in the following order: C. rubrum > C. corymbosum > C. officinalis w C. crinita > C. gracilis > E. intestinalis > C. barbata > C. vagabunda > U. rigida. Generally, red algae accumulated natural nuclides to higher concentrations, while there is no clear colour dependence of 210Pb accumulation in the other alga phyla. The measured nuclide content in Black Sea algae can be used also as a characterization of radionuclide level at different Bulgarian Black Sea coastal regions. The results for 226Ra and 210Pb algae are indicators for Ra and Pb quantities in seawater and sediments. These data can be used for comparison of the different geographical regions of the Bulgarian Black Sea shore from north to south (presented in Fig. 2). Judging from the 226Ra content (9– 39 Bq/kg) in the red alga C. rubrum, the studied locations can be arranged: Rusalka < Bjala < Maslen nos < Perla < Ahtopol < Sinemoretz < Shabla < Rezovo < Varvara < Ravda < Kaliakra < Tuzlata. The 210Pb concentrations in C. rubrum from all samples were in the range 4–41 Bq/kg. It should be noted that 210Pb content was higher than its parent 226Ra in Ravda, Maslen nos, Ahtopol and Rezovo (highest in Ravda) probably due to fresh sediment deposits carried by the seawater currents. The data show that red algae selectively accumulated 210Pb and 226 Ra to a measurable extent from U series. Al-Masri (2002) reports also that red algae in the Mediterranean accumulate 210Pb and radium isotopes to higher levels and this is an indication for their affinity towards these isotopes.
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A. Strezov, T. Nonova / Journal of Environmental Radioactivity 100 (2009) 144–150
ROMANIA
N Shabla Rusalka Tuzlata
Kaliakra
Varna Bjala
BLACK SEA
Ravda
Burgas
Rossenetz Maslen Nos Perla Varvara Ahtopol Sinemoretz Rezovo
TURKEY
Fig. 1. Sampling locations along the Bulgarian Black Sea coast.
Higher natural nuclide values were measured at Rossenetz (226Ra – 118 Bq/kg and 210Pb – 190 Bq/kg) where high values were measured at the beach and in the bay sediments (137Cs content is also higher 34 Bq/kg). This site is known for the high content of natural nuclides which are a by-product of the exploitation of a copper mine in the vicinity. The effect of phosphate ore unloading operations may be the cause of higher 226Ra and 210Pb values in the beaches, sediments and biota from Shabla, Tuzlata and Kaliakra sites (Varna bay) and Ravda (Burgas bay), but local mineral contribution should not be neglected. A recent study supported by IAEA was performed to assess the impact of unloading cargoes of phosphate ore from ships,
showing the impact on the near marine environment at the Mediterranean sea coast (Al-Masri, 2002). Such activities are performed also at Bulgarian seaports and, together with mining activities in some places, led to a higher natural nuclide content at the beaches, in sea sediments and biota. Data were obtained in some of the studied algae species for 232 Th series nuclides – 228Ac, 208Tl. The concentrations of the nuclides were low, varying between 1 and 7 Bq/kg for 228Ac and 1 and 3 Bq/kg for 208Tl. The 228Th concentrations were close to the lower limit of detection (LLD) level (same as 234Th), meaning that daughters of 238U are more readily accumulated compared to 232Th.
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147
Table 2 Radionuclide accumulation in green, brown and red Black Sea macroalgae (in Bq/kg dry wgt; N – number of samples). Algae
137
226
Cs
N
210
Ra
40
Pb
K
Mean SD
Range
Mean SD
Range
Mean SD
Range
Mean SD
Range
Green algae Ulva rigida Enteromorpha intestinalis Cladophora vagabunda Chaetomorpha gracilis Bryopsis plumosa
14 9 11 5 5
4.1 0.7 3.3 0.8 4.0 0.8 2.3 0.8 2.1 0.6
1.5–10 1.4–7 2.0–9 1.2–5.3 1.4–4.1
81 82 12 2 72 900 120
3–16 3–15 4–18 4–11 650–1300
61 10 2 81 11 2 63 18
3–15 3–15 3–14 5–16 45–100
596 62 690 60 1300 180 1860 200 740 90
460–985 370–1230 520–2330 1220–2500 570–870
Brown algae Cystoseira barbata Cystoseira crinita
18 21
6.1 0.5 5.3 0.4
3–10 2.6–10
12 2 81
3–17 2–17
91 12 1
3–18 2–21
1350 190 1530 90
130–1980 1340–1990
Red algae Ceramium rubrum Callithamnion corymbosum Corallina officinalis
23 6 8
9.7 0.8 4.4 0.7 2.4 0.5
4–18 2.9–6.5 1.2–5.4
21 2 62 61
9–39 3–17 2–11
16 2 13 4 12 2
4–41 4–30 4–22
1343 98 1580 110 140 10
860–2100 1230–1920 124–170
The highest measured natural nuclide concentrations were determined in the green alga Bryopsis plumosa (Table 2, Fig. 3). This is one of the widespread Black Sea green macrophytes and it differs from the other algae because of its life cycle and maximum of development in winter. This green alga seems to extract some of 238 U daughters – 226Ra, 210Pb and 232Th daughters – 228Ra, 228Ac, 208 Tl, 212Bi, 212Pb from the seawater up to 1000–2000 Bq/kg level that is approximately three orders of magnitude higher than all other alga species collected from the same site. Dovlete (1990), tras¸cu (1995) also report the high Dovlete and Osvath (1992) and Pa natural radionuclide content in the green B. plumosa. Variations of 137Cs, 226Ra, 210Pb concentration depending on sampling year for C. rubrum from all sampling sites are presented in Fig. 4. The observed 137Cs, 226Ra and 210Pb concentrations have been almost constant (except 2001–2002). 3.2. Metals The mean values for Fe varied in the range 80–3530 mg/kg, the highest measured mean content was 1500 mg/kg in green Cladophora sp. Manganese ranged 7–350 mg/kg – with the highest, 180 mg/kg, in Chaetomorpha sp. (Table 3). The element Cu is one of the most biologically important metals and its compounds usually exist in the biosphere only in trace quantities, participating in the biological circle. Increase of Cu content may lead to a substantial damage in living organisms. The Cu concentration variations were in the range of 1–18 mg/kg for green and brown algae while for the red species the range was 3– 26 mg/kg. These data are close to the range obtained by other authors (Campanella et al., 2001; Topcuog˘lu et al., 2001) for
Fig. 2. Mean
226
Ra and
210
Pb content in Ceramium rubrum.
analogous algae species from neighboring seas (Mediterranean, Marmara, etc.) with exception of C. officinalis (8.5–26.4 mg/kg). The data for Zn, Cr, Pb and Cd were in the range 7–48 mg/kg, 0.5–24.6 mg/kg, 0.6–7.6 mg/kg and 0.2–2.9 mg/kg, respectively. Zinc forms different inorganic and organic complexes in seawater and about 50% of Zn is in the form of free ion in surface waters (Bruland, 1983). Sulphide forms of Zn prevail in greater depths of the Black Sea sediments (Landing and Lewis, 1991). The metals Cr, Cd and Pb are among the major hazardous contaminants in ecosystems – Cr is in the form of complexes bound by metalo-enzymes, leading to its accumulation by biota in high concentrations. Cadmium is toxic and poisonous for living organisms even in low concentrations. The behavior of Pb in water is complex and it is found in seawaters mainly in the form of different organic compounds. The results (histogram of mean values, data range) for trace metals in the three macrophytic phyla are compared in Fig. 5. All macroalgae species accumulated Cd, Cu, Pb and Zn to a similar extent, while the red and green algae have similarity in Cr and Mn content. The data show that the red algae species (Rhodophyta) accumulate metals higher than the other phyla (except Fe whose values are higher in green algae because of the chlorophyll). All data for the whole Bulgarian coast (about 300 km long) obtained from 13 sampling sites distributed from northern border to southern are evaluated by multivariable cluster analysis – Ward’s method (STATISTICA for Windows, StatSoft Inc., 1998, www.statsoft. com). Cluster analysis for the red C. rubrum data is presented because this alga is abundant along the whole Bulgarian Black Sea coast and accumulates metals to considerable concentrations. The results of the statistical analysis led to grouping in three clusters of all 12 Ceramium sp. sampling locations, depending on 4 radionuclides and 7 metals (about 80 samples) for the whole 1996–2004 period (Fig. 6a). In the first cluster are the locations with the highest measured 137Cs, 226Ra and 40K concentrations – Maslen nos, Perla, Kaliakra and Tuzlata. These sites are divided in two subgroups (Maslen nos, Perla and Kaliakra, Tuzlata), whose grouping is clear because of geographical proximity and similarity in the sediments matrix – slime. The southern sites Ahtopol, Varvara and Sinemoretz (þcentral Ravda) comprise the second cluster having lower nuclide concentrations than the first cluster (here also similarity in the sediment matrix – sand). The third cluster with the lowest concentrations – Shabla, Sinemoretz, Rusalka and Bjala also connects sites with sand matrix which sorbes nuclides to the lowest level. Mean nuclide values in the determined clusters are presented in Table 4. Second cluster contains sites with highest mean 210Pb concentrations (mainly in the south) which is in conformity with the presence of metal mines from antiquity in the region.
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2200
Ra-226
2000
Pb-210
Bryopsis plumosa Mean; Whisker: Min, Max
Ac-228
1800
Ra-224 1600
Tl-208
Bq/kg
1400 1200 1000 800 600 400 200 0
Ahtopol 1996
Shabla 1999
Shabla 1998
Rusalka 2003
Shabla 2003
Fig. 3. Radionuclide content in green algae Bryopsis plumosa.
60 55 50 45
Cs-137
Mean; Whisker: Min, Max
Ra-226 Pb-210
40
Bq/kg
35 30 25 20 15 10 5 0
1996
1998
1999
2000
2001
2002
2003
2004
Fig. 4. Radionuclide content in macrophytes for different sampling years.
Table 3 Trace metals in macroalgae species (mean SD (range in parentheses) in mg/kg). Element (mg/kg)
Chlorophyta Ulva rigida
Enteromorpha intestinalis
Cladophora vagabunda
Chaetomorpha gracilis
Bryopsis plumosa
Cystoseira barbata
Cystoseira crinita
Ceramium rubrum
Callithamnion corymbosum
Corallina officinalis
Cd
0.8 0.2 (0.3–2.1) 1.8 0.4 (0.5–3.2) 5.6 0.9 (2.2–10.9) 430 90 (110–1000) 35 8 (9–108) 1.6 0.1 (1.2–1.8) 16 3 (7–32)
0.8 0.2 (0.3–1.6) 5.3 0.9 (1.9–8.6) 71 (1.3–10.5) 1010 80 (190–1940) 47 8 (21–71) 2.4 0.2 (1.7–3.2) 14 1 (10–17)
1.0 0.3 (0.3–2.9) 71 (1.8–25) 61 (4–16) 1500 310 (810–3530) 170 20 (38–350) 3.5 0.7 (1.7–7.5) 19 4 (8–48)
1.3 0.3 (0.5–2.9) 71 (2–14) 51 (2–9) 520 80 (160–880) 180 20 (100–230) 2.7 0.3 (1.2–4.6) 12 2 (6–18)
0.40 0.06 (0.25–0.42) 71 (4–10) 81 (1–18) 340 30 (310–400) 60 10 (26–94) 3.8 0.6 (1.7–7.6) 19 4 (9.4–31)
0.32 0.03 (0.20–0.43) 2.3 0.6 (0.7–5.7) 51 (1.4–9.2) 440 90 (120–790) 47 9 (7–86) 1.4 0.2 (0.6–2.1) 17 2 (8–26)
0.44 0.06 (0.24–0.75) 3.9 0.7 (1.3–6.5) 72 (3.8–17) 260 60 (80–450) 32 9 (11–97) 1.7 0.2 (1.2–2.4) 20 3 (12–33)
0.8 0.1 (0.3–1.3) 6.1 1.4 (0.8–16.5) 7.6 0.8 (3.4–12.2) 850 150 (140–1890) 121 22 (30–320) 2.2 0.3 (1.3–3.8) 22 3 (7–39)
0.53 0.20 (0.2–1.2) 3.7 0.6 (1.6–5.6) 5.4 0.9 (2.8–8.5) 880 70 (290–1850) 87 15 (33–200) 2.3 0.4 (1.4–3.6) 18 3 (11–25)
0.73 0.24 (0.4–1.2) 4.8 0.3 (1.3–10.8) 15 2 (8.5–26) 600 40 (280–800) 55 9 (35–88) 1.4 0.1 (1.3–1.5) 13 2 (10–15)
Cr Cu Fe Mn Pb Zn
Phaeophyta
Rhodophyta
A. Strezov, T. Nonova / Journal of Environmental Radioactivity 100 (2009) 144–150
70
400 350
Cu
60
300
Mn
50
250
Zn
Cd Cr Pb Rb
40
mg/kg
mg/kg
149
200 150
Zr 30 20
100 10
50 0
0
-50
-10
Rhodophyta
Phaeophyta
Chlorophyta
Chlorophyta
Rhodophyta
Phaeophyta
Fig. 5. Mean content of trace metals in algae phyla.
Tree Diagram for 12 Cases Ward`s method, Euclidean distances
Tree Diagram for 12 Cases Ward`s method, Euclidean distances Shabla Sinemoretz Rusalka Bjala Ravda Ahtopol Varvara Rezovo Tuzlata Kaliakra Maslen nos Perla
Shabla Sinemoretz Rusalka Rezovo Bjala Ravda Ahtopol Maslen nos Varvara Tuzlata Kaliakra Perla
radionuclides
0
1
2
3
4
5
6
7
metals
1
2
3
4
5
6
7
8
Linkage Distance
Linkage Distance Fig. 6. Cluster analysis of contaminants in Ceramium rubrum.
There is a resemblance between the cluster diagrams of nuclides and metals because nuclides are also trace metal contaminants that both have an impact on biota in marine ecosystems. The grouping of locations shows logical geographic dependence of contaminant content together with separation of clean areas. The tree diagram for metals in C. rubrum contains two major clusters. The first (as for nuclides) contains geographically close sites Kaliakra, Tuzlata plus Perla with higher content. The second cluster is divided in two subparts whose variation values are close. The lower metal content is in Shabla, Rusalka, Bjala, Sinemoretz and Rezovo which are situated in the far north and south parts of the Black Sea coast. Mean metal values in C. rubrum obtained for the different clusters are given in Table 5.
4. Conclusions Radionuclide and metal accumulation capacity has been studied in three algae phyla along the Bulgarian Black Sea coast during the period 1996–2004. The red alga C. rubrum had the highest 137Cs
Table 4 Mean nuclide values, obtained for Ceramium rubrum by clusters [Bq/kg]. Nuclide
Cluster I [(Maslen nos, Perla) þ (Kaliakra, Tuzlata)]
Cluster II {[(Ahtopol, Varvara) þ Rezovo] þ Ravda}
Cluster III [(Shabla, Sinemoretz) þ (Rusalka, Blala)]
137
12.6 21 14 1639
7.9 17 20 1104
7.6 14 6 1285
Cs Ra Pb 40 K 226 210
levels. The green B. plumosa accumulated natural radionuclides by three orders of magnitude higher than other algae sampled from the same locations. B. plumosa is one of the widespread Black Sea macrophytes and differs from the other studied algae by the life cycle (winter) and maximum of development. This alga seems to extract preferably some of 238U daughters – 226Ra, 210Pb and 232Th daughters 228Ra, 228Ac, 208Tl. The data show that there is no serious contamination of the Bulgarian coast with radionuclides, as no nuclear activities have been carried out in the region. Elevated natural nuclide levels were mostly due to mining of phosphate ores and minerals, carried out in the vicinity of sampling sites. The status of the marine environment in all studied areas was evaluated by cluster analysis of macroalgae data from all geographic zones. Results showed a geographical distribution of contaminants in tree diagrams for radionuclides and metals. The elevated levels were mainly due to Danube, Dnieper and Dnester Table 5 Mean metal values, obtained for Ceramium rubrum by clusters [mg/kg]. Element Cluster I Cluster II.1 Cluster II.2 [(Tuzlata, Kaliakra) {[(Ahtopol, Ravda) {[(Sinemoretz, Rusalka) þ Perla] þ Maslen nos] þ Varvara} þ Shabla] þ Rezovo} þ Bjala Cd Cr Cu Fe Mn Pb Rb Sr Zn
1.06 9.6 10.7 1490 443 2.9 11 206 34
0.57 3.9 9.3 565 92 1.6 10 155 25
1.04 5.7 4.4 681 128 2.2 13 128 15
150
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