Fish Reproduction Is Disrupted upon Lifelong Exposure to Environmental PAHs Fractions Revealing Different Modes of Action

Abstract

Polycyclic aromatic hydrocarbons (PAHs) constitute a large family of organic pollutants emitted in the environment as complex mixtures, the compositions of which depend on origin. Among a wide range of physiological defects, PAHs are suspected to be involved in disruption of reproduction. In an aquatic environment, the trophic route is an important source of chronic exposure to PAHs. Here, we performed trophic exposure of zebrafish to three fractions of different origin, one pyrolytic and two petrogenic. Produced diets contained PAHs at environmental concentrations. Reproductive traits were analyzed at individual, tissue and molecular levels. Reproductive success and cumulative eggs number were disrupted after exposure to all three fractions, albeit to various extents depending on the fraction and concentrations. Histological analyses revealed ovary maturation defects after exposure to all three fractions as well as degeneration after exposure to a pyrolytic fraction. In testis, hypoplasia was observed after exposure to petrogenic fractions. Genes expression analysis in gonads has allowed us to establish common pathways such as endocrine disruption or differentiation/maturation defects. Taken altogether, these results indicate that PAHs can indeed disrupt fish reproduction and that different fractions trigger different pathways resulting in different effects.

Fish life-history traits are affected after chronic dietary exposure to an environmentally realistic marine mixture of PCBs and PBDEs

“…We acknowledge that the results reported here using a freshwater species may not fully apply to marine fish, especially when considering the additional metabolic costs due to osmotic pressure maintenance in an hyperosmotic environment. There are however a large number of articles reporting similar toxicity pathways in marine and freshwater fish species for a number of biological functions such as growth (Bodiguel et al, 2009;Daouk et al, 2011), behavior (Gravato and Guilhermino, 2009;Oliveira et al, 2012;Vignet et al, 2017) and reproduction (Sun et al, 2015;Vignet et al, 2016). These studies therefore support the hypothesis that the present results on a freshwater fish species are indicative of what could happen in marine fish.…”

“…For instance, Muirhead et al (2006) showed that exposure to BDE-47 caused a significant reduction in mature sperm in fathead minnows, suggesting that PBDEs can affect male reproductive function and reduce male fertility. In the present study, the delayed increase in reproductive output observed in MIX fish could also be explained by such disruption caused by PCBs and PBDEs producing a delay in follicle maturation as this has been shown after exposure to PCBs (Daouk et al, 2011) or PAHs (Vignet et al, 2016).…”

“…However, the effect of a mixture of PCBs and PBDEs may differ from those assessed for a single type of POPs (Daouk et al, 2011) or a single congener (Han et al, 2013) because of potentially differing mechanisms of action between PCBs and PBDEs as well as synergistic and antagonistic effects. In addition, fertilization can be highly variable within one treatment, which makes mean fertilization rate a poor predictor (Vignet et al, 2016).…”

Comprehensive review of polycyclic aromatic hydrocarbons in water sources, their effects and treatments

“…Among acquired immune parameters, lymphocyte proliferation is extremely sensitive to polycyclic aromatic hydrocarbon exposure. Vignet et al (2016) found that PAHs might disrupt fish reproduction. Additionally, Balcıog˘lu (2016) reported that occupational exposure to high levels of contaminant mixtures comprising PAH resulted in symptoms such as eye irritation, vomiting, convulsion and nausea; however, it was not known which of the mixture components were responsible for these effects.…”

Hypoxia and reduced salinity exacerbate the effects of oil exposure on sheepshead minnow (Cyprinodon variegatus) reproduction

“…We have previously demonstrated that exposure to crude oil highenergy water accommodated fraction (HEWAF; an environmentally relevant PAH mixture), results in reduced egg production by SHM and developmental effects in two generations of offspring (Jasperse et al, 2019). Many other studies have also reported reproductive impairment in fish exposed to PAHs, including reduced egg production (Brown-Peterson et al, 2013;Raimondo et al, 2016;Vignet et al, 2016), reduced serum estradiol levels (Pollino et al, 2009) delayed spawning and spermiation (Khan, 2012), and altered testicular development (Sundt and Bjorkblom, 2011). However, it remains unknown how adverse environmental conditions common to estuarine environments affect the sensitivity of SHM to the reproductive effects of HEWAF.…”