Unveiling the neurotoxicity of methylmercury in fish ( Diplodus sargus ) through a regional morphometric analysis of brain and swimming behavior assessment

Abstract

The current study aims to shed light on the neurotoxicity of MeHg in fish (white seabream - Diplodus sargus) by the combined assessment of: (i) MeHg toxicokinetics in the brain, (ii) brain morphometry (volume and number of neurons plus glial cells in specific brain regions) and (iii) fish swimming behavior (endpoints associated with the motor performance and the fear/anxiety-like status). Fish were surveyed for all the components after 7 (E7) and 14 (E14) days of dietary exposure to MeHg (8.7μgg), as well as after a post-exposure period of 28days (PE28). MeHg was accumulated in the brain of D. sargus after a short time (E7) and reached a maximum at the end of the exposure period (E14), suggesting an efficient transport of this toxicant into fish brain. Divalent inorganic Hg was also detected in fish brain along the experiment (indicating demethylation reactions), although levels were 100-200 times lower than MeHg, which pinpoints the organic counterpart as the great liable for the recorded effects. In this regard, a decreased number of cells in medial pallium and optic tectum, as well as an increased hypothalamic volume, occurred at E7. Such morphometric alterations were followed by an impairment of fish motor condition as evidenced by a decrease in the total swimming time, while the fear/anxiety-like status was not altered. Moreover, at E14 fish swam a greater distance, although no morphometric alterations were found in any of the brain areas, probably due to compensatory mechanisms. Additionally, although MeHg decreased almost two-fold in the brain during post-exposure, the levels were still high and led to a loss of cells in the optic tectum at PE28. This is an interesting result that highlights the optic tectum as particularly vulnerable to MeHg exposure in fish. Despite the morphometric alterations reported in the optic tectum at PE28, no significant changes were found in fish behavior. Globally, the effects of MeHg followed a multiphasic profile, where homeostatic mechanisms prevented circumstantially morphometric alterations in the brain and behavioral shifts. Although it has become clear the complexity of matching brain morphometric changes and behavioral shifts, motor-related alterations induced by MeHg seem to depend on a combination of disruptions in different brain regions.

Mercury in Juvenile Solea senegalensis: Linking Bioaccumulation, Seafood Safety, and Neuro-Oxidative Responses under Climate Change-Related Stressors

“…Such differences can be mostly attributed to the fact that (i) each fish tissue is functionally and structurally different, thus having distinct baseline biomarker/enzyme levels and responding differently to environmental stressors, including their interactions [80], (ii) different Hg concentrations were reached in each tissue (i.e., liver > brain > muscle), and (iii) chemical contaminants, like the neurotoxic Hg, can have specific modes of action and target organs [64]. Hence, despite the significantly higher Hg concentrations found in the liver, the present findings show that neuro-oxidative responses triggered by Hg were more notorious in the brain (i.e., significant differences were found between non-contaminated and Hg contaminated fish in LPO, CAT, SOD, and AchE activities, and negative correlations between these variables and Hg NAR occurred in this tissue, a result that is consistent with the mode of action (neurotoxic) of this contaminant (e.g., Reference [84]).…”

Oxidative stress profiles in brain point out a higher susceptibility of fish to waterborne divalent mercury compared to dietary organic mercury

“…The considerable decrease of tHg in brain of D. sargus at PE28 in the MeHg exposure is most probably due to its elimination. This hypothesis is supported by results from a parallel study that reported a very low percentage (< 1.5%) of Hg in the brain of fish exposed to MeHg was in the form of Hg(II), suggesting low amounts of demethylation (Puga et al, 2016). After 28 days of depuration, levels in the brain decreased to half of those recorded at E14.…”

“…However, there are fundamental knowledge gaps concerning the effects of mercury species on the fish brain. This is an important issue since fish fitness and survival are significantly affected by the neurotoxic effects of Hg exposure (Farina et al, 2013;Pereira et al, 2016;Puga et al, 2016).…”

“…While there are a few studies on the neurotoxicity of MeHg in fish (Berntssen et al, 2003;Puga et al, 2016), there is very little information on the ability of divalent mercury [Hg(II)] to accumulate in fish brain and the resulting effects. The primary focus on MeHg in the literature is likely due to the perception of its higher toxicity associated with rapid uptake and partitioning to sensitive tissues such as the brain.…”

Mercury in the tissues of five cephalopods species: First data on the nervous system

“…The present study provided information regarding the bioaccumulation and tissue distribution of Hg Basu et al, 2005;Zahir et al, 2005;Puga et al, 2016), and induces oxidative stress responses (Mieiro et al, 2011), no information has been reported regarding Hg neurotoxicity in cephalopods to date. Since Hg concentrations of some E. cirrhosa specimens (i.e.…”