Benzo[a]pyrene Effects on Reproductive Endpoints in Fundulus heteroclitus

Abstract

Benzo[a]pyrene (BaP) is a polycyclic aromatic hydrocarbon (PAH) that has been implicated in modulating aromatase enzyme function with the potential to interrupt normal reproductive function. The aim of this study was to use a fish model, Fundulus heteroclitus, to assess whether BaP exposure adversely impacts reproduction. Adult fish were exposed to waterborne BaP nominal concentrations of (0, 1, or 10 μg/l) for 28 days. Males and females were combined for the second half of the exposure (days 14-28) in order to quantitate egg production and fertilization success. Egg fertilization and subsequent hatching success of F1 embryos was significantly decreased by the high dose of BaP. In males, both gonad weight and plasma testosterone concentrations were significantly reduced compared to controls by 10 μg/l BaP. Histopathological examination of testes including spermatogonia, spermatocyte and spermatid cyst areas, percentage of cysts per phase, and area of spermatozoa per seminiferous tubule were not significantly affected. Other biomarkers, including male liver weight, liver vitellogenin (vtg) mRNA expression and sperm concentrations, were also not affected. In females, estradiol concentrations were significantly reduced after BaP exposure, but egg production, gonad weight, liver weight, vtg expression and oocyte maturation were not altered. Steroid concentrations in Fundulus larvae from exposed parents at 1 and 3 weeks posthatch were not significantly changed. BaP exposure at these environmentally relevant concentrations caused negative alterations particularly in male fish to both biochemical and phenotypic biomarkers associated with reproduction and multigenerational embryo survival.

Transgenerational effects of polycyclic aromatic hydrocarbon exposure on sheepshead minnows (Cyprinodon variegatus)

“…Our data bolster the growing body of evidence that hydrocarbon exposure can alter egg production in female fish (Brown‐Peterson et al ; Perrichon et al ; Raimondo et al ) and decrease reproductive fitness in male fish by reducing fertilization rate (Booc et al ). Hydrocarbons have also been shown to reduce sperm quantity (Sundt and Bjorkblom ) and quality (Nagler and Cyr ) and delay spermiation (Khan ), though those endpoints were not assessed in the present study.…”

“…The present study demonstrated an array of transgenerational effects, including F 1 developmental changes and impaired F 2 prey capture ability. Other studies have demonstrated developmental effects in fish embryos and larvae exposed to PAHs (White et al ; Incardona et al ; Booc et al ), including reduced hatch frequency, decreased survival, and cardiac abnormalities. A study investigating the developmental effects of PAH exposure on zebrafish embryos found that phenanthrene, a 3‐ring PAH, caused cardiac dysfunction, including bradycardia and arrhythmias, and pyrene, a 4‐ring PAH, caused reduced blood circulation, anemia, and neuronal cell death (Incardona et al ).…”

“…Although many studies have established the toxicity of hydrocarbons (individual or mixtures) on fish reproductive and developmental functions (Villeneuve et al ; Incardona et al ; Reynaud and Deschaux ; Dubansky et al ; Booc et al ; Brown‐Peterson et al ; Beyer et al ; Hedgpeth and Griffitt ; Raimondo et al ), few have investigated multi‐ or transgenerational effects. Furthermore, most generational studies use a chronic exposure across all generations tested, which may not be an environmentally relevant parallel to exposure during an oil spill when it is possible that only the parental generation (F 0 ) is exposed.…”

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

“…Therefore, results will be globally discussed in the light of relevant studies which have, however, mostly been performed using individual PAHs. Indeed, exposures to individual PAHs have been shown to reduce the number of eggs in several fish species [ 19 , 39 , 40 , 41 , 42 ] while an exposure to benzo[a]pyrene produced a decreased fertilization rate in mummichog [ 43 ]. In contrast, an exposure of Japanese medaka to phenanthrene produced no modification of the daily number of eggs spawned and fertilization rate did not change, with the exception of one intermediate concentration [ 17 ].…”

Long-Term Exposure to Benzo[a]Pyrene Affects Sexual Differentiation and Embryos Toxicity in Three Generations of Marine Medaka (Oryzias Melastigma)

“…Corrales et al [13] have found that BaP can affect the growth and development of zebrafish offspring. Meanwhile, Booc et al [14] also found that the decreased embryos fertilization and hatching success of Fundulus heteroclotus were caused by BaP exposure. Moreover, some studies suggest that the expression of key genes has changed in some important pathways, which promote the toxic effects of BaP in fish, especially at critical development and reproductive stages [15].…”