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Aquatic Toxicology Olfactory Toxicity in Fishes Aquatic Toxicology 96 (2010) 2–26 Contents lists available at ScienceDirect Aquatic Toxicology journal homepage: www.elsevier.com/locate/aquatox Review Olfactory toxicity in fishes Keith B. Tierney a, David H. Baldwin b, Toshiaki J. Hara c,d, Peter S. Ross e, Nathaniel L. Scholz b, f, Christopher J. Kennedy ∗ a Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9 Canada b Environmental Conservation Division, Northwest Fisheries Science Center, NOAA Fisheries, 2725 Montlake Blvd. East, Seattle, WA 98112-2097, United States c Department of Fisheries and Oceans, 501 University Crescent, Winnipeg, MB, R3T 2N6 Canada d Department of Zoology, University of Manitoba, Winnipeg, MB, R3T 2N2 Canada e Institute of Ocean Sciences, Department of Fisheries and Oceans, 9860 West Saanich Rd., Sidney, BC, V8L 4B2 Canada f Department of Biological Sciences, Simon Fraser University, Burnaby, BC, V5A 1S6 Canada article info abstract Article history: Olfaction conveys critical environmental information to fishes, enabling activities such as mating, locat- Received 11 November 2008 ing food, discriminating kin, avoiding predators and homing. All of these behaviors can be impaired or Received in revised form 1 September 2009 lost as a result of exposure to toxic contaminants in surface waters. Historically, teleost olfaction studies Accepted 5 September 2009 have focused on behavioral responses to anthropogenic contaminants (e.g., avoidance). More recently, there has been a shift towards understanding the underlying mechanisms and functional significance of Keywords: contaminant-mediated changes in fish olfaction. This includes a consideration of how contaminants affect Olfaction the olfactory nervous system and, by extension, the downstream physiological and behavioral processes Fish Contaminants that together comprise a normal response to naturally occurring stimuli (e.g., reproductive priming or Metals releasing pheromones). Numerous studies spanning several species have shown that ecologically rel- Neurotoxicity evant exposures to common pollutants such as metals and pesticides can interfere with fish olfaction Behavior and disrupt life history processes that determine individual survival and reproductive success. This rep- resents one of the pathways by which toxic chemicals in aquatic habitats may increasingly contribute to the decline and at-risk status of many commercially and ecologically important fish stocks. Despite our emerging understanding of the threats that pollution poses for chemical communication in aquatic communities, many research challenges remain. These include: (1) the determination of specific mecha- nisms of toxicity in the fish olfactory sensory epithelium; (2) an understanding of the impacts of complex chemical mixtures; (3) the capacity to assess olfactory toxicity in fish in situ; (4) the impacts of toxins on olfactory-mediated behaviors that are still poorly understood for many fish species; and (5) the connec- tions between sublethal effects on individual fish and the long-term viability of wild populations. This review summarizes and integrates studies on fish olfaction-contaminant interactions, including metrics ranging from the molecular to the behavioral, and highlights directions for future research. © 2009 Elsevier B.V. All rights reserved. Contents 1. Introduction .......................................................................................................................................... 3 2. Fish olfaction ......................................................................................................................................... 3 3. Olfactory toxicity..................................................................................................................................... 5 3.1. Molecular and biochemical indicators of olfactory toxicity ................................................................................. 5 3.2. Neurophysiological indicators of olfactory toxicity.......................................................................................... 11 3.2.1. pH ................................................................................................................................... 11 Abbreviations: 11-KT, 11 ketotestosterone; ABS, alkyl benzene sulfonates; ACh, acetylcholine; AChE, acetylcholinesterase; BKME, bleached kraft pulpmill effluent; CYP, cytochrome P450; DOC, dissolved organic carbon; EEG, electro-encephalogram; EOG, electro-olfactogram; GPCR, G-protein coupled receptor; GSH, glutathione; GST, glutathione S-transferase; GtH II, gonadotropin II; KME, unbleached kraft pulpmill effluent; LC50, median lethal concentration; OB, olfactory bulb; OE, olfactory epithelium; OP, organophosphate insecticides; OSN, olfactory sensory neuron; PGF, F-type prostaglandin; ppb, parts per billion; ppm, parts per million; SLS, sodium laurel sulfonate; TChA, taurocholic acid; WHO, whole crude oil; WSF, water-soluble fraction of crude oil. ∗ Corresponding author. Tel.: +1 778 782 5640. E-mail address: [email protected] (C.J. Kennedy). 0166-445X/$ – see front matter © 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.aquatox.2009.09.019 K.B. Tierney et al. / Aquatic Toxicology 96 (2010) 2–26 3 3.2.2. Metals ............................................................................................................................... 11 3.2.3. Pesticides ........................................................................................................................... 11 3.2.4. Other contaminants ................................................................................................................ 13 3.3. Anatomical indicators of olfactory toxicity .................................................................................................. 13 3.3.1. pH ................................................................................................................................... 13 3.3.2. Metals ............................................................................................................................... 13 3.3.3. Pesticides ........................................................................................................................... 13 3.3.4. Other contaminants ................................................................................................................ 13 3.4. Behavioral indicators of olfactory toxicity ................................................................................................... 13 3.4.1. pH ................................................................................................................................... 16 3.4.2. Metals ............................................................................................................................... 16 3.4.3. Pesticides ........................................................................................................................... 16 3.4.4. Other contaminants ................................................................................................................ 18 3.5. Integrating neurophysiological, physiological, and behavioral data ........................................................................ 18 3.6. Challenges in separating physiologic and olfactory responses .............................................................................. 22 4. Endpoints related to olfactory toxicity .............................................................................................................. 22 5. Olfactory toxicity endpoints vs. other toxicity endpoints ........................................................................................... 22 6. Research directions .................................................................................................................................. 23 7. Conclusion............................................................................................................................................ 23 Acknowledgements .................................................................................................................................. 24 References ........................................................................................................................................... 24 1. Introduction situationally inappropriate cues. Some contaminants may appear to affect olfaction, but are actually impairing responses that can be Fish rely upon olfaction to provide invaluable information over linked to olfaction, such as directed swimming. Because of this com- long distances and through environmental conditions that can plexity, isolating the manner(s) in which any given toxicant affects render other sensory modalities unavailable. To receive olfactory olfaction can require assessment of numerous biological endpoints. information, sensory neurons interface almost directly with the It is important to note that even though concentrations of con- aquatic environment, typically protected only in a covered cavity by taminants in the environment are typically quite low (e.g. in the mucous. In such an exposed situation, dissolved contaminants can ppb), they are not necessarily below concentrations of other com- interact with the olfactory neurons as readily as odorants, which pounds known to elicit biological responses (Fig. 3). For example, 9 is problematic given many of the contaminants presently found in for three classes of odorants, a concentration of 10− M is suffi- the world’s
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