Concentration of OCPs residues in samples of Astyanax altiparanae captured in the Alagados dam in Ponta Grossa
The results of the mean concentrations of Aldrin, p, p'-DDT, p, p'-DDE, Dieldrin, α-endosulfan and β-endosulfan are shown in Table 2 to 4.
Table 2
Mean concentrations of OCPs under study in Astyanax altiparanae muscle
Samples | Aldrin | α-Endosulfan | p, pꞌ-DDE | Dieldrin | β-Endosulfan | p, pꞌ-DDT |
1 (ng/g) | <LOD | 4.2 ± 0.7f | 12.7 ± 11.9d | <LOD | 8.6 ± 2.2e | 16.4 ± 8.4b |
2 (ng/g) | <LOD | <LOD | <LOD | <LOD | 34.7 ± 21.8b | 22.3 ± 0.2a |
3 (ng/g) | <LOD | <LOD | <LOD | <LOD | 4.4 ± 2.7e | <LOD |
4 (ng/g) | <LOD | <LOD | <LOD | <LOD | 11.3 ± 9.8c | 23.1 ± 13.1a |
5 (ng/g) | <LOD | <LOD | <LOD | <LOD | 58.5 ± 28.7a | <LOD |
6 (ng/g) | <LOD | 4.6 ± 1.3e | 15.5 ± 8.7c | <LOD | 12.0 ± 3.5d | <LOD |
7 (ng/g) | 8.3 ± 0.5d | <LOD | 15.3 ± 3.3c | <LOD | <LOD | <LOD |
8 (ng/g) | <LOD | <LOD | <LOD | <LOD | 20.6 ± 8.9c | <LOD |
9 (ng/g) | <LOD | 4.7 ± 0.3d | 20.1 ± 1.7b | <LOD | <LOD | <LOD |
10 (ng/g) | <LOD | 12.3 ± 3.4b | 13.4 ± 2.6d | <LOD | 20.1 ± 9.1c | 12.8 ± 11.6c |
11 (ng/g) | <LOD | <LOD | 16.8 ± 0.2c | <LOD | <LOD | <LOD |
12 (ng/g) | 9.1 ± 0.1c | <LOD | <LOD | <LOD | <LOD | <LOD |
13 (ng/g) | 26.1 ± 0.2ª | 18.9 ± 12a | 40.2 ± 4.5a | 45.60 ± 2.01a | <LOD | 20.7 ± 9.7a |
14 (ng/g) | 13.1 ± 5.7b | 9.5 ± 4.4c | 38.1 ± 9.1a | <LOD | 13.3 ± 2.9e | 12.0 ± 8.7c |
MRL (ng/g) | 200 | 100 | 5000 | 200 | 100 | 5000 |
Note: Maximum Residue Limit (MRL) source: FAO and WHO (2012). Values followed by the same letter do not differ statistically at the 95% level. |
It is possible to verify in Table 2 that the muscle of the collected specimens presented contamination by Aldrin (8.3 to 26. ng/g), α-endosulfan (4.2 to 12.3 ng/g), p, p'-DDE (12.7 to 40.2 ng/g), Dieldrin (45.6 ng/g), β-endosulfan (8.6 to 58.5 ng/g) and p, p'-DDT (12, 8 to 23.1 ng/g). These results are below the maximum residue limit stipulated by. Among the determined OCPs, it is noted in Table 3 that the one present in the highest concentrations is p, p'-DDE. However, these results are lower than those presented by Akan (2013) evaluated fish muscle, from a lake in Nigeria, regarding contamination by OCPs, verifying the presence of p, p'-DDE (4320 ng/g ), p, p'-DDT (2760 ng/g) and endosulfan (4810 ng/g). The results of determination of OCPs in fish muscle are similar to those reported by Barnhoorn et al. (2015), who detected p, p'-DDE, Aldrin and endosulfan in South African lakes. It has been found that greater than 80% of the total intake of pesticides residues by humans is through the food chain via consumption of contaminated food (Abbassy et al. 2021). The Astyanax altiparanae (Lambari) is one of the most consumed fish species in Brazil, with its muscles being the most consumed part. Consequently, these results demonstrate the risks that the consumption of these fish can pose to the population.
Table 3 shows contamination by OCPs in Astyanax altiparanae roe, collected at the Alagados reservoir.
Table 3
Mean concentrations of POPs under study in Astyanax altiparanae roe
Samples | Aldrin | α-Endosulfan | p, p'-DDE | Dieldrin | β-Endosulfan | p, p'-DDT |
1 (ng/g) | <LOD | 6.8 ± 3.8e | 33.6 ± 0.06f | 82.9 ± 11.5f | 6.0 ± 0.91f | 56.6 ± 26.9d |
2 (ng/g) | <LOD | 8.7 ± 2.5d | 134.7 ± 68.9a | <LOD | 23.3 ± 6.7c | <LOD |
3 (ng/g) | <LOD | 5.3 ± 1.5f | 92.3 ± 28.6c | 124.3 ± 20.5d | 10.2 ± 0.9e | <LOD |
4 (ng/g) | <LOD | 5.7 ± 0.2f | 113.5 ± 0.2b | 143.9 ± 0.1c | 15.4 ± 0.1d | <LOD |
5 (ng/g) | <LOD | 5.4 ± 0.6f | 24.2 ± 0.3g | 120.7 ± 49.9d | 51.6 ± 0.1a | <LOD |
6 (ng/g) | <LOD | <LOD | 24.4 ± 0.5g | 101.9 ± 21.6e | <LOD | 97.9 ± 12.2c |
7 (ng/g) | 30.8 ± 4.4d | 3.4 ± 0.6g | 4.2 ± 0.3i | 98.5 ± 27.5e | 10.3 ± 0.05e | 67.7 ± 23.2d |
8 (ng/g) | 48.9 ± 1.9c | 11.1 ± 3.8c | 46.1 ± 0.1e | 105.9 ± 31.6e | 31.4 ± 5c | 118.4 ± 0.8b |
9 (ng/g) | <LOD | 23.5 ± 15.0a | 17.3 ± 4.9h | 77.8 ± 19.9f | 43.8 ± 11.7b | 128.8 ± 0.4b |
10 (ng/g) | 17.07 ± 2.9e | 20.0 ± 0.7a | 61.0 ± 17.3d | 183.1 ± 0.6a | 6.8 ± 0.06f | 129.3 ± 1.1b |
11 (ng/g) | 63.6 ± 9.6b | 10.2 ± 0.3c | 11.3 ± 0.1h | 96.7 ± 0.1e | 13.8 ± 0.2d | <LOD |
12 (ng/g) | 50.6 ± 27.9c | 8.8 ± 4.2d | <LOD | 89.2 ± 2.1f | 35.8 ± 24.3c | 123.0 ± 20.8b |
13 (ng/g) | 74.0 ± 23.0a | 8.0 ± 1.1d | <LOD | 162.6 ± 70.5b | 16.4 ± 3.8d | 87.9 ± 4 5.0c |
14 (ng/g) | 22.3 ± 6.4e | 14.9 ± 0.2b | <LOD | 64.7 ± 1.4g | <LOD | 286.8 ± 5.6a |
MRL (ng/g) | 200 | 100 | 5000 | 200 | 100 | 5000 |
Note: Maximum Residue Limit (MRL) source: FAO and WHO (2012). Values followed by the same letter do not differ statistically at the 95% level. |
It can be seen in Table 3 that the Astyanax altiparanae roe samples analyzed showed contamination by Aldrin (17.07 to 50.6 ng/g), α-endosulfan (3.4 to 23.5 ng/g), p, p'-DDE (4.2 to 134.7 ng/g), Dieldrin (84.7 to 183. ng/g), β-
endosulfan (6.0 to 51.6 ng/g) and p, p'-DDT (56.6 to 286.8 ng/g). When comparing data on contamination by OCPs in roe (Table 4) with data obtained from muscle (Table 3), a higher concentration of OCPs in roe is observed. The percentage of fat in fish tissues varies according to the stage of life in which it is found. In the reproductive phase, when eggs are produced, lipids are mobilized from the liver and mainly from the muscle to the gonads (Castell et al. 1972). The most frequently analyzed tissues to verify contamination by OCPs in fish are usually muscle, liver and gills (Corrêa et al. 2022; Rohani 2023). Few studies evaluate the presence of OCPs in roes. Thus, these results contribute to a better understanding about the contamination of OCPs in this important organ and the implications that this can cause, such as the lack of development of these species. Their indirect effects may be related to their negative effects on the growth and survival rate of fish (Sabra et al. 2015). In addition, these roes serve as food for larger fish and can contribute to a process of biomagnification of these contaminants. Table 4 shows the mean concentrations of OCPs under study in Astyanax altiparanae viscera.
Table 4
Mean concentrations of OCPs under study in Astyanax altiparanae viscera
Samples | Aldrin | α-Endosulfan | p, pꞌ-DDE | Dieldrin | β-Endosulfan | p, pꞌ-DDT |
1 (ng/g) | 72.5 ± 9.2b | 37.0 ± 0.01a | <LOD | 193.5 ± 55.8a | 39.1 ± 14.5e | 89.2 ± 0.2a |
2 (ng/g) | 93.3 ± 0.1a | <LOD | <LOD | 155.4 ± 0.5c | <LOD | <LOD |
3 (ng/g) | 32.4 ± 0.2f | 33.0 ± 0.1a | 110.0 ± 0.1d | <LOD | 21.0 ± 0.2f | 52.3 ± 0.3b |
4 (ng/g) | <LOD | <LOD | <LOD | <LOD | <LOD | <LOD |
5 (ng/g) | 10.8 ± 0.2g | 8.7 ± 0.2d | <LOD | 61.8 ± 0.2f | <LOD | <LOD |
6 (ng/g) | 96.6 ± 0.3a | 8.3 ± 0.1d | <LOD | <LOD | <LOD | <LOD |
7 (ng/g) | 93.8 ± 3.7a | 35.4 ± 0.5a | <LOD | <LOD | 23.1 ± 0.2f | <LOD |
8 (ng/g) | 43.6 ± 0.1e | 28.5 ± 0.1b | 83.5 ± 0.1e | 18.0 ± 0.1g | 87.3 ± 0.7b | <LOD |
9 (ng/g) | <LOD | <LOD | <LOD | <LOD | 64.4 ± 1.2c | <LOD |
10 (ng/g) | <LOD | <LOD | <LOD | 136.4 ± 0.3d | 69.1 ± 2.3c | <LOD |
11 (ng/g) | 66.0 ± 18.3c | 31.2 ± 0.2b | 185.5 ± 0.5b | 179.0 ± 8.5b | 63.5 ± 0.7c | <LOD |
12 (ng/g) | 61.5 ± 7.0c | 24.7 ± 0.1c | 148.9 ± 2.5c | 155.5 ± 50.2c | 95.4 ± 16.3a | <LOD |
13 (ng/g) | 55.2 ± 0.4d | <LOD | 209.2 ± 0.3a | 137.7 ± 35.9d | 56.8 ± 4.8d | <LOD |
14 (ng/g) | 71.7 ± 18.1b | 29.5 ± 0.7b | 109.4 ± 0.5d | 87.2 ± 0.3e | 57.8 ± 1.0d | 57.3 ± 15.2b |
MRL (ng/g) | 200 | 100 | 5000 | 200 | 100 | 5000 |
Note: Maximum Residue Limit (MRL) source: FAO and WHO (2012). Values followed by the same letter do not differ statistically at the 95% level. |
It can be seen in Table 4 that the Astyanax altiparanae viscera samples analyzed showed contamination by Aldrin (19.8 to 93.3 ng/g), α-endosulfan (8.3 to 37 ng/g), p, p'-DDE (83.5 to 209.2 ng/g), Dieldrin (18 to 193. ng/g), β-endosulfan (21 to 95.4 ng/g) and p, p'-DDT (52.3 to 89.2 ng/g).
In different studies, higher concentrations of OCPs were obtained in fish viscera when compared to muscle and other tissues (Akan 2013; Gui et al. 2014) Of the pesticides analyzed, all, except p, p'-DDT, were detected in concentrations that varied, in general, as follows: Viscera > Roe > Muscle, The concentration range of Aldrin was 14.18 ng/g to 63.42 ng/g; Dieldrin, 45.6 ng/g to 124.97 ng/g; α-endosulfan and βendosulfan, 9.02 ng/g to 25.26 ng/g and 20.39 ng/g to 57.77 ng/g, respectively; and DDE and DDT, 21.5 ng/g to 141.08 ng/g and 17.87 ng/g to 121.86 ng/g, respectively.
Aldrin was detected at concentrations above the LOD limit in 78.6%, 50%, and 28.6% of the viscera, roe, and muscle samples, respectively. Dieldrin was detected at concentrations higher than the LOD limit in 92.9%, 64.3%, and 7.14% of the roe, viscera, and muscle samples, respectively; however, none of the samples exceeded the contamination limit of 200 ng/g stipulated by the US.EPA (2016) for Aldrin and Dieldrin.
Regarding concentration, p, pꞌ-DDE may represent both direct action and metabolic transformation from p, pꞌDDT to p, pꞌ-DDE in fish. Was verified that 78.6%, 57.14%, and 42.9% of the roe, muscle, and viscera samples, respectively, presented p, pꞌ-DDE contamination. The POP p, pꞌ-DDT was detected in 64.3%, 42.9%, and 21.4% of roe, muscle, and viscera samples, respectively; however, all concentrations were below the limit stipulated by FAO and WHO (2012), which is 500 ng/g.
Endosulfan was detected in 92.8%, 71.4%, and 64.3% of roe, viscera, and muscle samples of Astyanax altiparanae, respectively; however, the detected values were below the values stipulated by FAO and WHO (2012), which is 100 ng/g. The OCPs analyzed in relation to concentration levels, except for p, pꞌ-DDT, were detected in tissues in the following order: viscera > roe > muscle; for the p, pꞌ-DDT roe > viscera > muscle.
This order of accumulation of OCPs for Astyanax altiparanae is similar to that found in Cichlasoma dimerus, a species native to the Paraguay River, where higher concentrations of endosulfan were determined in the liver than in the muscle (Da Cuña et al. 2020). Barni et al. (2016) studied species with different eating habits and trophic levels in the shallow lake La Peregrina located in the southeast of the Pampa region, Argentina; the authors found higher concentrations of endosulfan in Odontesthes bonariensis (plankton feeder) and Oligosarcus jenynsii (carnivorous), following the pattern of concentration liver > gonads > muscle. The authors concluded that, these concentrations could be associated with the different feeding habits and trophic web levels occupied by the species. In addition, in this study, females of the species Cyphocharax voga (detritus and phytoplankton feeder) presented higher concentrations of DDT in the gonads than in the liver. This same pattern could also be observed for the species Micropterus salmoides, Hoplias malabaricus, Clarias gariepinus, Heterotis niloticus, Oreochromis niloticus, and Tilapia zilli collected in lakes and dams. These species showed a tendency to accumulate OCPs in viscera, such as liver, kidney, gastrointestinal tract, and gonads, compared with muscle among all species (Miranda et al. 2008; Akan 2013; Dang et al. 2016).
This concentration pattern for OCPs can be explained by the relationship between the lipophilic characteristics of pollutants and the lipid content of each tissue. After the viscera, the second tissue with the highest accumulation of OCPs was gonads in studies found in the literature. This is because lipid metabolism plays a fundamental role in the transfer of contaminants in the reproduction process, because the development of oocytes requires large amounts of lipids as an energy source for embryo development, and may contribute to embryonic contamination (Landrum and Fisher 1999, referencia 17 ).
It was also possible to observe that analyte p, pꞌ-DDT presented higher concentrations in the roe when compared to viscera, probably because p, pꞌ-DDT is dehalogenated in p, pꞌ-DDE under conditions of anaerobiosis in the gastrointestinal tract, justifying the higher concentration of p, pꞌ-DDE in the viscera (Huang et al. 2001; Kwong et al. 2008). The metabolization of DDT is a slow process, so part of this unmetabolized compound can be transferred to the roe, maintaining its original form (p, pꞌ-DDT). During the embryo development process, the necessary lipids are removed from maternal stocks or synthesized from maternal extrahepatic lipids (Landrum and Fisher 1999).The highest concentrations of Dieldrin may be related to the photolysis process of Aldrin in fish organs. Aldrin is converted into Dieldrin in plant and animal tissues. This is because Dieldrin is extremely nonpolar and, therefore, has a strong tendency to adsorb lipids such as animal fats and plant waxes (Chopra et al. 2011). Dieldrin is one of the most persistent chemicals known, and the bioaccumulation of Dieldrin in animal tissue is due to its metabolism, characterized by limited digestion and excretion. However, it is easily absorbed and transported throughout the bloodstream of vertebrates and hemolymph of invertebrates (Matsumura 1985).Table 5 presents the dimensions and mass of the analyzed specimens.
Table 5
Dimensions (cm) and body mass of Astyanax altiparanae individuals collected at the Alagados reservoir.
Samples | Length (mm) | Width (mm) | Mass (g) | | Samples | Length (mm) | Width (mm) | Mass (g) |
1 | 99 | 30 | 14.29 | | 8 | 95 | 28 | 11.93 |
2 | 102 | 27 | 15.15 | | 9 | 110 | 31 | 17.91 |
3 | 105 | 30 | 15.09 | | 10 | 100 | 27 | 13.77 |
4 | 103 | 28 | 14.91 | | 11 | 103 | 32 | 15.69 |
5 | 94 | 28 | 12.97 | | 12 | 109 | 32 | 17.27 |
6 | 102 | 31 | 17.14 | | 13 | 97 | 30 | 15.11 |
7 | 91 | 30 | 16.13 | | 14 | 103 | 31 | 16.84 |
Figure 2 Graph of scores (A) and loadings (B) for fish samples analyzed for PCA, the correlation between the width and contamination. Note: Red: smaller widths; Green: larger widths
In the PCA presented in Fig. 2A (scores), it is possible to verify the formation of a grouping highlighted by S; they concentrate 85.7% of the samples with the lowest body widths (red). Figure 2B (loadings), it can see that specimens with the highest width (green) have higher concentrations of analytes. Assuming that this result is related to the amount of body fat, that is, with a larger width, there is a greater fat deposit in their tissues, favoring the bioaccumulation of POPs. In addition, it may be an indication of a higher level of maturation of the specimens; in the final stage of maturation, before spawning, the abdomen of the females increases significantly.
Marcon et al. (2017) found that, even exposed to OCPs, fish roe maintains their physiological characteristics and the spawning occurs normally. However, these compounds can be transferred to offspring from the mother before birth or from the contaminated environment after birth. Environmental contamination by OCPs is a global problem. The Alagados Reservoir is not located near the site where the OCPs was used; however, even at relatively low concentrations, OCPs were detected in the tissues of Astyanax altiparanae. Atmospheric deposition can be classified as a potential pathway for contamination of aquatic ecosystems by OCPs. In addition, surface runoff, as a result of possible illegal use of these pesticides in adjacent areas, may also be a source of possible contamination (Bouwman et al. 2008; Bornman et al. 2017). The smuggling of pesticides is becoming an aggravating factor for environmental contamination. It is estimated that 20% of the consumption of pesticides in Brazil comes from smuggling, which is the storage and disposal of inadequate packaging. Considering the chemical composition, these irregularly produced pesticides may have the active ingredient in a concentration 600% higher than that of regulated pesticides, in addition to unknown and/or prohibited substances present in their formulation (IDESF 2019).
Risk assessment for human health
Table 6 presents the results of risk assessment in relation to consumption of Astyanax altiparanae from the Alagados Reservoir.
Table 6
Estimated daily intake (EDI); ng/Kg.d and hazard quotients (HQs) calculated based on average OCPs concentrations (ng/g wet weight) detected in the muscle, roe and viscera of Astyanax altiparanae, collected in the Alagados Reservoir, Brazil.
| | Muscle | Roe | Viscera |
Analytes | ADI (ng/Kg.d) | 50th (95th ) EDI percentile | 50th (95th ) RQP (10− 3) | 50th (95th ) EDI percentile | 50th (95th ) RQP (10− 3) | 50th (95th ) EDI percentile | 50th (95th ) RQP (10− 3) |
Aldrin | 100 | 9.2 (19.9) | (9) (91) | 40.2 (58.3) | 402 (585) | 54.3 (79.2) | 542 (792) |
α-Endosulfan | 6000 | 5.8 (14.2) | 0.9 (2.3) | 7.1 (17.6) | 1.1 (2.9) | 24.2 (29.9) | 4.0 (4.9) |
p, pꞌ-DDE | 10000 | 13.3 (32.4) | 1.3 (3.2) | 27.6 (102) | 2.7 (10.1) | 106.4 (167) | 10.6 (16.7) |
Dieldrin | 100 | 37.5 (37.5) | 374 (374) | 85.4 (139.5) | 853 (1390) | 113.1 (154.3) | 1131 (1543) |
β-Endosulfan | 6000 | 10.9 (40.3) | 1.8 (6.7) | 13.1 (38.9) | 2.1 (6.4) | 49.8 (75.4) | 8.3 (12.5) |
p, pꞌ-DDT | 10000 | 15.2 (18.8) | 1.5 (1.8) | 97.3 (184) | 9.7 (18.4) | 47.1 (70.7) | 4.7 (7.0) |
Note: EDI values are compared with USEPA acceptable daily intake (ADI) values. HQ values in bold exceed those of Health Canada guidelines. RQP: Risk quotient percentile. |
The contamination data presented here reflect the availability of OCPs for biological absorption within the study area and indicates the concentrations to which humans may be exposed at the time of ingestion. The levels of OCPs detected in Astyanax altiparanae samples did not exceed the maximum residue limits (MRLs) imposed by FAO and WHO (2012).
The estimated daily intake for the OCPs studied showed that all EDI values, except for Dieldrin, in percentile concentration were below the ADI values stipulated by the USEPA (Table 6). However, the calculated risk quotient (HQ) values indicated that Dieldrin in muscle, roe, and viscera samples exceeded the limit value of 0.2 at percentile concentrations 50 and 95. These data indicate health risks associated with the consumption of Astyanax altiparanae, although a more detailed risk assessment is required to verify the likely impact on human health. Other studies on fish tissues have obtained similar results related to the risk of Dieldrin and Aldrin for human health (Buah-Kwofie et al. 2018).
However, even if p, pꞌ-DDE residues do not reach the MRLs imposed by regulatory bodies, there is evidence that correlates the presence of p, pꞌ-DDE (1.26 ng/mL) in umbilical cord blood with the reduction of thyroid stimulator hormone, TSH, in three-day old boys (Dufour et al. 2018). Thus, the concentration of p, pꞌ-DDE found in this study indicates that there is risk in the consumption of these fish, as these pesticides are classified as endocrine disruptors can act as weak hormones, they bind to receptors located on the plasma membrane producing a non-genomic steroid action. In this context, concentrations at physiological levels may be more effective than concentration at toxic levels (Vandenberg et al. 2012).
The risks evaluated here may not bring immediate changes to consumers, although the risk estimates presented are a preliminary assessment of the increased susceptibility to intoxication by consumption of Astyanax altiparanae from this location.
Finally, the importance of monitoring and controlling the degree of contamination of the PRB by OCPs residues should be highlighted, since the waters belonging to this basin contribute significantly to the formation of other, even larger bodies of water, such as the Tibagi, Paranapanema and Paraná rivers. In addition, the entire basin is located under the Guaraní aquifer, which is one of the world's largest sources of fresh water. The accumulation of these substances, even at trace levels, can cause irreversible environmental damage and compromise water resources in the future.