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. 2022 Jul 10;12(14):1766.
doi: 10.3390/ani12141766.

Aquatic Pollution and Risks to Biodiversity: The Example of Cocaine Effects on the Ovaries of Anguilla anguilla

Mayana Karoline Fontes  1   2 , Luigi Rosati  3   4 , Mariana Di Lorenzo  3 , Camilo Dias Seabra Pereira  2 , Luciane Alves Maranho  5 , Vincenza Laforgia  3 , Anna Capaldo  3   4
Affiliations

Aquatic Pollution and Risks to Biodiversity: The Example of Cocaine Effects on the Ovaries of Anguilla anguilla

Mayana Karoline Fontes et al. Animals (Basel). .

Abstract

Pollution is one of the main causes of the loss of biodiversity, currently one of the most important environmental problems. Important sources of aquatic pollution are illicit drugs, whose presence in waters is closely related to human consumption; their psychoactive properties and biological activity suggest potential adverse effects on non-target organisms, such as aquatic biota. In this study, we evaluated the effect of an environmentally relevant concentration of cocaine (20 ng L−1), an illicit drug widely found in surface waters, on the ovaries of Anguilla anguilla, a species critically endangered and able to accumulate cocaine in its tissues following chronic exposure. The following parameters were evaluated: (1) the morphology of the ovaries; (2) the presence and distribution of enzymes involved in oogenesis; (3) serum cortisol, FSH, and LH levels. The eels exposed to cocaine showed a smaller follicular area and a higher percentage of connective tissue than controls (p < 0.05), as well as many previtellogenic oocytes compared with controls having numerous fully vitellogenic and early vitellogenic oocytes. In addition, the presence and location of 3β-hydroxysteroid dehydrogenase, 17β-hydroxysteroid dehydrogenase, and P450 aromatase differed in the two groups. Finally, cocaine exposure decreased FSH and LH levels, while it increased cortisol levels. These findings show that even a low environmental concentration of cocaine affects the ovarian morphology and activity of A. anguilla, suggesting a potential impact on reproduction in this species.

Keywords: Anguilla anguilla; cocaine; gonadotropins; oogenesis enzymes; ovary.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Figure 1
Figure 1
Light micrographs of Anguilla anguilla ovaries. Mallory staining. (A–D) control specimens. The ovary showed numerous fully vitellogenic oocytes (fvOos) and early vitellogenic oocytes (evOos), along with few previtellogenic oocytes (pvOos) and connective interfollicular cells (arrowheads). (E–H) Exposed specimens, containing more connective tissue (arrows) and previtellogenic oocytes (pvOos) than the control specimens. FC, follicular cells; *, theca cells. Scale bars: (A,E) = 100 μm; (B) = 50 μm; (C,D,F–H) = 5 μm.
Figure 2
Figure 2
Histomorphometric analysis of Anguilla anguilla ovaries. (A) Percentage of connective tissue relative to gonad area; in the exposed eels, connective tissue occupied a larger area in the gonads than the control animals. (B) Mean area of follicles; follicles in the gonads from the exposed eels were smaller than those in the controls. (C) Number of follicles present within the gonads; no differences in the number of follicles were found between the exposed and control specimens. (*) Significantly different (p < 0.05) from control values.
Figure 3
Figure 3
Light micrographs of Anguilla anguilla ovaries from control (A–C) and exposed (D–F) specimens. Immunolabeling with anti-3β-HSD antibody. (A–C) a wide and strong positive reaction (arrow) was visible at the level of the fully vitellogenic oocytes (fvOos) and early vitellogenic oocytes (evOos); a weak signal was evident in the follicular (FCs) and theca cells (*) as well as in the connective tissue (arrowheads). (D–F) Previtellogenic oocytes (pvOos) and early vitellogenic oocytes (evOos) were immunolabeled. In these cells, the immunohistochemical signal was in the cytoplasm as spots (arrow). A weak signal was evident in the connective cells (arrowheads). No positivity was found in the follicular (FCs) or theca (*) cells. (F) (insert) Negative control: no labeling was evident in the ovary. Bars: (A) = 20 μm; (B,C,E,F) = 5 μm, (D) = 50 μm, (F) (inset) = 100 μm.
Figure 4
Figure 4
Light micrographs of Anguilla anguilla ovaries from control (A–C) and exposed specimens (D–F). Immunolabeling with anti-17β-HSD antibody. (A–C) a wide and strong positive reaction was present in fully vitellogenic oocytes (fvOos) and early vitellogenic oocytes (evOos); a weak signal was evident in the follicular (FCs) and theca (*) cells as well as in the connective cells (arrowheads). (D–G) early vitellogenic oocytes (evOos) were immunolabeled, and the signal was in some areas of the cytoplasm as spots (arrow); meanwhile, weak positivity (arrow) was localized within previtellogenic oocytes (pvOos), follicular (FC), and connective cells (arrowheads). No signal was evident in the theca cells (*). (E) (insert) negative control: no labeling was evident in the ovary. Bars: (A) = 20 μm; (B,C,E–G) = 5 μm, (D) = 50 μm, (E) (inset) = 100 μm.
Figure 5
Figure 5
Light micrographs of Anguilla anguilla ovaries from control (A–D) and exposed specimens (E–G). Immunolabeling with anti-P450 aromatase antibody. (A–D) a wide and strong positive reaction was present in fully vitellogenic oocytes (fvOos) and early vitellogenic oocytes (evOos), as well as in the follicular (FCs), theca (*), and connective cells (arrowheads). (E–G) previtellogenic (pvOos) and early vitellogenic oocytes (evOos) were immunolabeled, and the signal was in some areas of the cytoplasm as spots (arrow); positivity was also found in the theca (*) and connective cells (arrowheads), while no signal was seen in the follicular cells (FCs). (F) (insert) negative control. No labeling was evident in the ovary. Bars: (A) = 20 μm; (B–D,F,G) = 5 μm, (E) = 50 μm, (F) (inset) = 100 μm.
Figure 6
Figure 6
Serum LH, FSH, and cortisol levels in Anguilla anguilla control and exposed specimens. Cocaine exposure decreased LH and FSH levels and increased cortisol levels. Values are means ± SD of the mean. (*) serum significantly different (p < 0.05) from the control values.
Figure 6
Figure 6
Serum LH, FSH, and cortisol levels in Anguilla anguilla control and exposed specimens. Cocaine exposure decreased LH and FSH levels and increased cortisol levels. Values are means ± SD of the mean. (*) serum significantly different (p < 0.05) from the control values.
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