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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.

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Date
2016-01
Authors
Brown, DR
Bailey, JM
Oliveri, AN
Levin, ED
Di Giulio, RT
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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.
Type
Journal article
Subject
Adaptive costs
Behavior
Fundulus heteroclitus
Locomotion
Polycyclic aromatic hydrocarbons (PAHs)
Subteratogenic
Adaptation, Biological
Animals
Dose-Response Relationship, Drug
Embryo, Nonmammalian
Embryonic Development
Environment
Exploratory Behavior
Fundulidae
Heart Defects, Congenital
Larva
Locomotion
Polycyclic Aromatic Hydrocarbons
Reflex, Startle
Statistics, Nonparametric
Time Factors
Water Pollutants, Chemical
Permalink
https://hdl.handle.net/10161/12417
Published Version (Please cite this version)
10.1016/j.ntt.2015.10.007
Publication Info
Brown, DR; Bailey, JM; Oliveri, AN; Levin, ED; & Di Giulio, RT (2016). 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. Neurotoxicol Teratol, 53. pp. 55-63. 10.1016/j.ntt.2015.10.007. Retrieved from https://hdl.handle.net/10161/12417.
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Scholars@Duke

Di Giulio

Richard T. Di Giulio

Sally Kleberg Distinguished Professor of Environmental Toxicology
Dr. Di Giulio serves as Director of Duke University's Integrated Toxicology Program and the Superfund Basic Research Center. Dr. Di Giulio's research is concerned with basic studies of mechanisms of contaminant metabolism, adaptation and toxicity, and with the development of mechanistically-based indices of exposure and toxicity that can be employed in biomonitoring. The long term goals of this research are to bridge the gap between mechanistic toxicological research and the development of usef
Levin

Edward Daniel Levin

Professor in Psychiatry and Behavioral Sciences
Dr. Levin is Chief of the Neurobehavioral Research Lab in the Psychiatry Department of Duke University Medical Center. His primary academic appointment is as Professor in the Department of Psychiatry and Behavioral Sciences. He also has secondary appointments in the Department Pharmacology and Cancer Biology, the Department of Psychological and Brain Sciences and the Nicholas School of the Environment at Duke. His primary research effort is to understand basic neural interactions underlyi
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