title: Developmental exposure to a complex PAH mixture causes persistent behavioral effects in naive Fundulus heteroclitus (killifish) but not in a population of PAH-adapted killifish.
abstract: Acute exposures to some individual polycyclic aromatic hydrocarbons (PAHs) and complex PAH mixtures are known to cause cardiac malformations and edema in the developing fish embryo. However, the heart is not the only organ impacted by developmental PAH exposure. The developing brain is also affected, resulting in lasting behavioral dysfunction. While acute exposures to some PAHs are teratogenically lethal in fish, little is known about the later life consequences of early life, lower dose subteratogenic PAH exposures. We sought to determine and characterize the long-term behavioral consequences of subteratogenic developmental PAH mixture exposure in both naive killifish and PAH-adapted killifish using sediment pore water derived from the Atlantic Wood Industries Superfund Site. Killifish offspring were embryonically treated with two low-level PAH mixture dilutions of Elizabeth River sediment extract (ERSE) (TPAH 5.04 μg/L and 50.4 μg/L) at 24h post fertilization. Following exposure, killifish were raised to larval, juvenile, and adult life stages and subjected to a series of behavioral tests including: a locomotor activity test (4 days post-hatch), a sensorimotor response tap/habituation test (3 months post hatch), and a novel tank diving and exploration test (3months post hatch). Killifish were also monitored for survival at 1, 2, and 5 months over 5-month rearing period. Developmental PAH exposure caused short-term as well as persistent behavioral impairments in naive killifish. In contrast, the PAH-adapted killifish did not show behavioral alterations following PAH exposure. PAH mixture exposure caused increased mortality in reference killifish over time; yet, the PAH-adapted killifish, while demonstrating long-term rearing mortality, had no significant changes in mortality associated with ERSE exposure. This study demonstrated that early embryonic exposure to PAH-contaminated sediment pore water caused long-term locomotor and behavioral alterations in killifish, and that locomotor alterations could be observed in early larval stages. Additionally, our study highlights the resistance to behavioral alterations caused by low-level PAH mixture exposure in the adapted killifish population. Furthermore, this is the first longitudinal behavioral study to use killifish, an environmentally important estuarine teleost fish, and this testing framework can be used for future contaminant assessment.
authors.affiliation: Nicholas School of the Environment, Duke University, Durham, NC 27514, USA. Electronic address: daniel.r.browndu@gmail.com.
authors.forename: D R
authors.initials: DR
authors.lastname: Brown
authors.affiliation: Duke University Medical Center, Duke University, Durham, NC 27514, USA.
authors.forename: J M
authors.initials: JM
authors.lastname: Bailey
authors.affiliation: Duke University Medical Center, Duke University, Durham, NC 27514, USA.
authors.forename: A N
authors.initials: AN
authors.lastname: Oliveri
authors.affiliation: Nicholas School of the Environment, Duke University, Durham, NC 27514, USA; Duke University Medical Center, Duke University, Durham, NC 27514, USA.
authors.forename: E D
authors.initials: ED
authors.lastname: Levin
authors.affiliation: Nicholas School of the Environment, Duke University, Durham, NC 27514, USA.
authors.forename: R T
authors.initials: RT
authors.lastname: Di Giulio
mesh_terms: D000220:Adaptation, Biological / Q000187:drug effects*; D000818:Animals; D004305:Dose-Response Relationship, Drug; D004625:Embryo, Nonmammalian / Q000002:abnormalities* / Q000187:drug effects; D047108:Embryonic Development / Q000187:drug effects*; D004777:Environment; D005106:Exploratory Behavior / Q000187:drug effects; D023781:Fundulidae; D006330:Heart Defects, Congenital / Q000139:chemically induced; D007814:Larva / Q000187:drug effects; D008124:Locomotion / Q000187:drug effects*; D011084:Polycyclic Aromatic Hydrocarbons / Q000633:toxicity*; D013216:Reflex, Startle / Q000187:drug effects; D018709:Statistics, Nonparametric; D013997:Time Factors; D014874:Water Pollutants, Chemical / Q000633:toxicity*
chemical_list: D011084:Polycyclic Aromatic Hydrocarbons; D014874:Water Pollutants, Chemical
keywords: Adaptive costs; Behavior; Fundulus heteroclitus; Locomotion; Polycyclic aromatic hydrocarbons (PAHs); Subteratogenic