Bioaccumulation of Arsenic Species in Rays from the Northern Adriatic Sea
Abstract
:1. Introduction
2. Results
2.1. Total Arsenic
Species/Max. DW * | Sample | DW * (cm) | DL # (cm) | TL ** (cm) | W ## (kg) | Sex | As (liver, µg·g−1) | As (muscle, µg·g−1) |
---|---|---|---|---|---|---|---|---|
Pteromylaeus bovinus/male cca. 90 cm, female max. 222 cm | 029PB | 52.8 | 30.2 | 87.5 | 1.50 | juv m | 9.1 ± 0.3 | 36.3 ± 0.5 |
034PB | 73.5 | 43.5 | 121.0 | 5.28 | m | 13.2 | 65.9 ± 0.8 | |
052PB | 113.5 | 71.5 | 194.0 | 21 | m | 18.7 | 92.3 | |
053PB | 163.0 | 108.0 | 196.0 | 74 | f | 30.2 ± 4.7 | 205 ± 5 | |
054PB | 188.5 | 118.0 | 224.0 | 110 | f | 34.6 | 222 ± 1 | |
055PB | 156.9 | 108.2 | 169.0 | 68 | f | 44.8 | 225 | |
056PB | 154.0 | 108.0 | 250.0 | 57 | f | 35.3 ± 1.9 | 148 ± 2 | |
057PB | 191.0 | 132.0 | 294.0 | 116 | f | 53.4 | 362 ± 10 | |
058PB | 222.0 | 115.5 | 267.0 | 88 | f | 30.6 | 222 ± 5 | |
060PB & | 53.5 | 12.4 | 87.9 | 1.88 | juv m | 12.2 | 107 ± 1 | |
062PB & | 57.1 | 33.5 | 86.0 | 2.52 | juv m | 11.3 | 57.8 ± 1.3 | |
063PB | 75.0 | 39.5 | 126.1 | 5.28 | f | 9.4 | 59.2 ± 0.8 | |
064PB | 77.5 | 41.1 | 125.6 | 6.20 | m | 10.5 ± 0.1 | - | |
066PB | 171.0 | 112.5 | 263.0 | 84 | f | 28.7 ± 2.4 | 180 ± 1 | |
067PB | 159.0 | 110.0 | 266.0 | 68 | f | 63.5 | 233 ± 1 | |
Min | - | 52.8 | 12.4 | 86.0 | 1.5 | - | 9.1 | 36.3 |
Max | - | 222.0 | 132.0 | 294.0 | 116 | - | 63.5 | 362 |
Myliobatis aquila/cca. 150 cm | 023MA | - | - | - | - | - | - | 51.4 |
025MA & | 38.0 | 22.5 | 67.0 | 0.98 | f | 19.9 ± 1.0 | 69.8 | |
028MA & | 34.5 | 21.2 | 64.0 | 0.62 | juv | 21.3 ± 1.7 | - | |
035MA & | 27.7 | 16.0 | 52.5 | 0.30 | m | - | 32.4 | |
044MA & | 27.3 | 14.5 | 49.5 | 0.26 | juv | - | 47.1 | |
061MA & | 27.5 | 14.2 | 52.5 | 0.32 | juv | - | 36.5 | |
Min | - | 27.3 | 14.2 | 49.5 | 0.26 | - | - | 32.4 |
Max | - | 38.0 | 22.5 | 52.5 | 0.98 | - | 69.8 | |
Pteroplatytrygon violacea/cca. 60 cm | 006PV | 60.0 | 54.9 | 139.2 | 7.56 | f | 26.3 ± 0.1 | 90.4 |
007PV | 56.2 | 42.0 | 137.5 | 5.44 | f | 34.8 | 48.3 | |
010PV | 55.0 | 42.5 | 129.0 | 5.22 | f | 40.7 | 82.4 ± 1.6 | |
038PV | 54.1 | 39.3 | 128.1 | 5.48 | f | 17.3 | 141 ± 4 | |
039PV | 44.5 | 34.0 | 107.0 | 2.64 | m | 23.8 ± 0.5 | 37.4 | |
049PV | 52.1 | 40.0 | 77.6 | 3.74 | m | 35.4 | 64.7 ± 0.2 | |
050PV | 58.8 | 45.0 | 126.2 | 6.12 | f | 34.4 ± 2.6 | 97.3 | |
051PV | 43.7 | 35.4 | 101.0 | 2.40 | m | 40.4 | 44.0 | |
Min | - | 43.7 | 34.0 | 77.6 | 2.4 | - | 17.3 | 37.4 |
Max | - | 60.0 | 54.9 | 139.2 | 7.56 | - | 40.7 | 97.3 |
Species | Sample | Astotal (µg·g−1) | Sum of Species (%) | AsIII (µg·g−1) | AsV (µg·g−1) | AB (µg·g−1) | DMA (µg·g−1) | Ether Extractable (µg·g−1) |
---|---|---|---|---|---|---|---|---|
Pteromylaeus bovinus | 029PB | 9.1 ± 0.3 | 40.6 | Traces ** | - | 1.57 ± 0.28 | 0.67 ± 0.08 | 1.44 |
034PB | 13.2 | 42.0 | traces | traces | 1.30 ± 0.17 | 1.47 ± 0.14 | 2.73 | |
052PB | 18.7 | 73.3 | traces | - | 6.75 ± 1.48 | 1.30 ± 0.13 | 5.64 | |
053PB | 30.2 ± 4.7 | 50.2 | traces | traces | 9.94 ± 0.76 | 1.79 ± 0.20 | 3.35 | |
054PB | 34.6 | 64. 6 | 0.04 ± 0.01 | - | 15.2 ± 2.8 | 1.33 ± 0.16 | 5.77 | |
055PB | 44.8 | 52.2 | 0.05 ± 0.01 | - | 12.0 ± 2.7 | 1.60 ± 0.16 | 9.76 | |
056PB | 35.3 ± 1.9 | 60.5 | 0.04 ± 0.01 | 0.16±0.08 | 17.2 ± 2.0 | 1.35 ± 0.15 | 2.60 | |
057PB | 53.4 | 69.2 | 0.04 ± 0.00 | - | 25.8 ± 0.3 | 2.22 ± 0.25 | 8.91 | |
058PB | 30.6 | 63.7 | 0.03 ± 0.01 | - | 11.0 ± 1.4 | 2.03 ± 0.34 | 6.44 | |
060PB | 12.2 | 44.4 | traces | - | 2.13 ± 0.14 | 0.89 ± 0.22 | 2.39 | |
062PB | 11.3 | 48.1 | traces | - | 1.58 ± 0.34 | 0.76 ± 0.02 | 3.09 | |
063PB | 9.4 | 45.5 | traces | - | 1.41 ± 0.20 | 0.84 ± 0.16 | 2.01 | |
064PB | 10.5 ± 0.2 | 47.1 | 0.03 ± 0.01 | - | 1.83 ± 0.16 | 1.27 ± 0.09 | 1.82 | |
066PB | 28.7 ± 2.4 | 69.0 | 0.03 ± 0.02 | 0.45 ± 0.40 | 12.4 ± 2.0 | 2.60 ± 0.22 | 4.33 | |
067PB | 63.5 | 70.9 | 0.05 ± 0.01 | - | 31.5 ± 3.3 | 2.06 ± 0.23 | 11.4 | |
Min | - | 9.1 | 40.6 | traces | - | 1.30 | 0.67 | 1.44 |
Max | - | 63.5 | 70.9 | 0.05 | - | 31.5 | 2.60 | 11.4 |
Myliobatis aquila | 025MA | 19.9 ± 1.0 | 46.9 | - | - | 3.13 ± 1.05 | 0.87 ± 0.11 | 5.33 |
028MA | 21.3 ± 1.7 | 43.7 | - | - | 4.36 ± 0.37 | 1.35 ± 0.07 | 3.60 | |
Pteroplatytrygon violacea | 006PV | 26.3 ± 0.2 | 65.4 | - | - | 9.91 ± 1.84 | 1.52 ± 0.19 | 5.78 |
007PV | 34.8 | 61.2 | - | - | 9.06 ± 0.39 | 3.09 ± 0.13 | 9.15 | |
010PV | 40.7 | 69.4 | traces | - | 17.5 ± 1.9 | 2.64 ± 0.26 | 8.09 | |
038PV | 17.3 | 79.1 | - | - | 6.10 ± 0.55 | 1.20 ± 0.17 | 6.38 | |
039PV | 23.8 ± 0.5 | 67.5 | - | - | 3.79 ± 0.96 | 1.75 ± 0.18 | 10.5 | |
049PV | 35.4 | 77.1 | traces | - | 14.8 ± 0.6 | 2.02 ± 0.19 | 10.5 | |
050PV | 34.4 ± 2.6 | 69.8 | traces | - | 13.6 ± 1.1 | 2.55 ± 0.38 | 7.84 | |
051PV | 40.4 | 47.6 | - | - | 10.4 ± 1.0 | 1.97 ± 0.1 | 6.86 | |
Min | - | 17.3 | 47.6 | 0.00 | - | 3.79 | 1.2 | 5.78 |
Max | - | 40.7 | 79.1 | traces | - | 17.5 | 3.09 | 10.5 |
2.2. Arsenic Speciation in Tissues
Species | Sample | Astotal | Astotal in Extract (%) | AsIII (µg/g) | AB (µg/g) |
---|---|---|---|---|---|
Pteromylaeus bovinus | 029PB | 36.3 ± 0.5 | 100 ± 6.0 | - | 30.7 ± 3.7 |
034PB | 65.9 ± 0.8 | 95.4 ± 2.1 | - | 54.8 ± 2.7 | |
052PB | 92.3 | 88.2 ± 1.5 | - | 74.9 ± 9.8 | |
053PB | 205 ± 4 | 78.5 ± 3.1 | traces ** | 152 ± 9.5 | |
054PB | 222 ± 2 | 79.2 ± 3.4 | traces | 190 ± 40 | |
055PB | 225 | 80.4 ± 2.8 | traces | 115 ± 5 | |
056PB | 148 ± 2 | 75.0 ± 4.9 | traces | 111 ± 2.0 | |
057PB | 362 ± 9 | 69.9 ± 5.1 | traces | 212 ± 28 | |
058PB | 222 ± 5 | 79.3 ± 4.5 | traces | 164 ± 17 | |
060PB | 107 ± 2 | 88.6 ± 1.7 | - | 82.6 ± 2.6 | |
062PB | 57.8 ± 1.3 | 82.9 ± 3.8 | - | 41.9 ± 5.8 | |
063PB | 59.2 ± 0.8 | 95.9 ± 3.9 | - | 53.0 ± 2.0 | |
066PB | 180 ± 0.5 | 81.1 ± 3.4 | traces | 122 ± 6 | |
067PB | 233 ± 2 | 79.8 ± 2.7 | traces | 185 ± 23 | |
Min | - | 36.3 | - | 0.00 | 30.7 |
Max | - | 362 | - | traces | 212 |
Myliobatis aquila | 023MA | 51.4 | 87.5 ± 3.3 | - | 33.2 ± 3.8 |
025MA | 69.8 | - | traces | 34.6 ± 3.4 | |
035MA | 32.4 | 84.6 ± 2.2 | - | 25.3 ± 2.0 | |
044MA | 47.1 | 85.8 ± 3.0 | traces | 27.8 ± 0.7 | |
061MA | 36.5 | 86.3 ± 2.5 | - | 29.4 ± 8.6 | |
Min | - | 32.4 | - | 0.00 | 25.3 |
Max | - | 69.8 | - | traces | 34.6 |
Pteroplatytrygon violacea | 006PV | 90.4 | 91.9 ± 8.0 | 0.03 | 80.6 ± 10.4 |
007PV | 48.3 | 69.6 ± 3.0 | - | 30.9 ± 0.3 | |
010PV | 82.4 ± 1.6 | 88.2 ± 2.1 | - | 75.3 ± 9.8 | |
038PV | 141 ± 4 | 73.8 ± 3.8 | 0.03 | 109 ± 10 | |
039PV | 37.4 | 88.8 ± 6.4 | traces | 30.1 ± 2.7 | |
049PV | 64.7 ± 0.5 | 82.8 ± 4.5 | traces | 39.1 ± 3.9 | |
050PV | 97.3 | 88.0 ± 3.4 | traces | 42.3 ± 3.7 | |
051PV | 44.0 | 88.9 ± 2.6 | - | 33.4 ± 1.2 | |
Min | - | 37.4 | - | 0.00 | 30.1 |
Max | - | 141 | - | 0.03 | 109 |
Variables | DW | DL | TL | W | As-Muscle | As-Liver | AB-Liver |
---|---|---|---|---|---|---|---|
As-muscle | 0.8862 * | 0.8948 * | 0.8555 * | 0.9254 * | - | 0.6112 * | - |
AB-muscle | 0.9006 * | 0.8942 * | 0.8817 * | 0.9206 * | 0.9577 * | - | 0.6698 * |
As-liver | 0.4902 * | 0.6218 * | 0.5797 * | 0.5724 * | - | - | - |
AB-liver | 0.5684 * | 0.6871 * | 0.6964 * | 0.6346 * | - | 0.9370 * | - |
DMA-liver | 0.2261 | 0.3253 | 0.3756 | 0.2661 | - | 0.6641 * | 0.5815 * |
Ether extract-liver | 0.1148 | 0.2375 | 0.2034 | 0.1910 | - | 0.7578 * | 0.6276 * |
Unextracted -liver | 0.6464 | 0.6236 | 0.5370 | - | −0.2178 | 0.1573 | 0.0760 |
3. Discussion
3.1. Distribution and Speciation of Arsenic
Species/Life Style | Source of Data | Age | Liver As (µg·g−1) | Muscle As (µg·g−1) | Individual Ratio Muscle to Liver |
---|---|---|---|---|---|
P. bovinus-benthic | This study | Juvenile | 10.9 ± 1.6 (n = 3) | 67.0 ± 36.2 (n = 3) | 5.96 ± 2.50 (n = 3) |
Mature | 31.1 ± 16.9 (n = 12) | 183 ± 88 (n = 12) | 5.69± 1.18 (n = 12) | ||
M. Aquila-benthic | This study | Juvenile | 20.6 (n = 2) | 47.4 ± 14.7 (n = 5) | 3.50 (n = 1) |
P. violacea-pelagic | This study | Mature | 31.7 ± 8.3 (n = 8) | 75.7 ± 34.5 (n = 8) | 2.02 ± 0.83 * (n = 7) |
Rhinoptera steindachneri-benthic | [33] | Juvenile | 21.0–54.2 | 5.0–33.0 | - |
Mature | 27.2–101.8 | 15.1–99.2 | |||
Raja clavata-benthic | [34] | - | cca. 10–19 # (n = 10) | cca. 27–157 # (n = 10) | - |
Manta birostris-pelagic | [35] | - | cca. 0.4–0.5 # | cca. 0.7–2.6 # | - |
3.2. Bioaccumulation of Arsenic with Proposed Biomagnification of AB
4. Experimental Section
4.1. Samples
4.2. Sample Preparation
4.3. Reagents and Standards
4.4. Preparation of Extracts (Figure 3)
4.5. Arsenic Speciation Using HPLC-HGAFS
4.6. Total Arsenic Determination Using ICP-MS
4.7. Total Arsenic Determination Using Instrumental Neutron Activation Analysis (INAA)
4.8. Quality Assurance and Quality Control
5. Conclusions
- High arsenic concentrations in liver and especially in muscle of all three ray species studied were found.
- Higher arsenic levels were observed in muscle of both benthic species (Pteromylaeus bovinus, Myliobatis aquila) in comparison with the pelagic one (Pteroplatytrygon violacea).
- The main arsenic compounds found in muscle was AB and in liver AB, DMA and arsenolipids.
- The good correlations found between the length or weight of the fish and total arsenic, or AB, concentrations for muscle reflect important accumulation of AB with age, and according to wider knowledge of local arsenic/AB distribution also its biomagnification in the benthic food chains.
- Since the content and relations between specific osmoregulators in these ray species are not known (Yancey, personal communication) our finding of high AB levels point on favorable retention of glycine betaine and coincidentally also AB for the purpose of osmoregulation; this hypothesis needs further investigation. In fact we are missing basic biological (or better physiological) data for particular ray species.
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Šlejkovec, Z.; Stajnko, A.; Falnoga, I.; Lipej, L.; Mazej, D.; Horvat, M.; Faganeli, J. Bioaccumulation of Arsenic Species in Rays from the Northern Adriatic Sea. Int. J. Mol. Sci. 2014, 15, 22073-22091. https://doi.org/10.3390/ijms151222073
Šlejkovec Z, Stajnko A, Falnoga I, Lipej L, Mazej D, Horvat M, Faganeli J. Bioaccumulation of Arsenic Species in Rays from the Northern Adriatic Sea. International Journal of Molecular Sciences. 2014; 15(12):22073-22091. https://doi.org/10.3390/ijms151222073
Chicago/Turabian StyleŠlejkovec, Zdenka, Anja Stajnko, Ingrid Falnoga, Lovrenc Lipej, Darja Mazej, Milena Horvat, and Jadran Faganeli. 2014. "Bioaccumulation of Arsenic Species in Rays from the Northern Adriatic Sea" International Journal of Molecular Sciences 15, no. 12: 22073-22091. https://doi.org/10.3390/ijms151222073