Ion homeostasis and interrenal stress responses in juvenile Pacific herring, Clupea pallasi, exposed to the water-soluble fraction of crude oil

https://doi.org/10.1016/j.jembe.2005.02.021Get rights and content

Abstract

Juvenile Pacific herring, Clupea pallasi, were exposed both acutely (96 h) and chronically (9 weeks) to three concentrations of the water-soluble fraction (WSF) of North Slope crude oil. Mean (± S.E.) total PAH (TPAH) concentrations at the beginning of the acute exposure experiment were: 9.7 ± 6.5, 37.9 ± 8.6 and 99.3 ± 5.6 μg/L. TPAH concentrations declined with time and the composition of the WSF shifted toward larger and more substituted PAHs. Significant induction of hepatic cytochrome P450 content, ethoxyresorufin O-deethylase and glutathione-S-transferase activities in WSF-exposed fish indicated that hydrocarbons were biologically available to herring. Significant but temporary, elevations in plasma cortisol (4.9-fold and 8.5-fold increase over controls in the 40 and 100 μg/L groups, respectively), lactate (2.2-fold and 3.1-fold over controls in the 40 and 100 μg/L groups) and glucose (1.3-fold, 1.4-fold and 1.6-fold over controls in the 10, 40 and 100 μg/L groups) occurred in fish exposed acutely to WSF. All values returned to baseline levels by 96 h. Similar responses were seen with the first of several sequential WSF pulses in the chronic exposure study. Subsequent WSF pulses resulted in muted cortisol responses and fewer significant elevations in both plasma lactate and glucose concentrations. Hematocrit, leucocrit, hemoglobin concentration and liver glycogen content were not affected by acute or chronic WSF exposure. Plasma [Cl], [Na+] and [K+] were significantly higher in the 100 μg/L WSF-exposed group by 96 h compared to control fish, and continued to be elevated through the entire chronic exposure period. Unlike the measured stress parameters, ionoregulatory dysfunction was not modulated by WSF pulses. The results of this study suggest that chronic exposure to WSF affects at least two important physiological systems in herring: the ability of fish to maintain ion homeostasis and the interrenally-mediated organismal stress response.

Introduction

Petroleum-derived hydrocarbons are a major contributor to the contamination of aquatic environments. Approximately 5 million tons of crude oil from a variety of sources enters the marine environment each year (Neff, 1990). Typical concentrations of total hydrocarbons in contaminated marine coastal waters can be as high as 80 μg/L, with occasional reports of up to 500 μg/L in the Arabian Gulf (Badawy and Al-Harthy, 1991, Madany et al., 1994, Alkindi et al., 1996). Much attention has been paid to large crude petroleum spills and their visible surface effects, however, of more recent concern are the potential effects of dissolved hydrocarbons, which are the most available to marine biota (Neff and Anderson, 1981). Of particular interest are the polycyclic aromatic hydrocarbons (PAHs), which are known to produce a myriad of lethal and sublethal effects in a wide range of biota.

The potential effects of hydrocarbons on marine benthic and intertidal organisms have been the primary focus of research to date. Notwithstanding, organisms that spend some or most of their lifecycle in the pelagic environment, such as the Pacific herring (Clupea pallasi), may also be negatively impacted by exposure. The acute toxicity of oil and its components have been well documented for several teleosts (Anderson et al., 1974, Rice et al., 1987) and reported effects in larval and juvenile stages include morphological, histopathological and genetic damage (Brown et al., 1996, Hose et al., 1996, Kocan et al., 1996, McGurk and Brown, 1996, Norcross et al., 1996, Carls, 1987, Carls et al., 1999, Heintz et al., 1999). Recently, work on the potential mechanisms underlying the common suite of PAH-induced developmental abnormalities in fish have been undertaken (Incardona et al., 2004). Still, more information is certainly needed on sublethal effects to further predictions regarding the risks of exposure to pelagic populations.

The exposure of fish to sublethal concentrations of contaminants can disturb homeostasis and impose considerable stress on physiological systems. The stress responses in teleosts is well documented and involves a series of cellular (e.g. heat shock protein production), neuroendocrine (e.g. catecholamines and corticosteroid release), biochemical (hyperlacticemia and hyperglycemia) and organismal responses (e.g. reduced growth, predisposition to disease, impaired reproduction and a reduced capacity to tolerate subsequent stress [Adams, 1990]), depending on the stressor and duration of its imposition.

Several reasons prompted an examination of the neuroendocrine and biochemical stress responses of juvenile Pacific herring exposed acutely and chronically to the WSF of crude oil. First, the paradigm of the neuroendocrine stress response is well documented in teleosts, and generally yields a consistent pattern for xenobiotic stressors. Second, fish are exposed to dissolved pollutants via an extensive respiratory surface and, in seawater, also by drinking. The high bioavailability of many chemicals in water, in combination with a variety of highly sensitive perceptive mechanisms in the integument, typically generate an integrated stress response in fish in addition to toxic effects. The ability of fish to mount an appropriate stress response, and the negative consequences associated with chronic stress, give its measurement both evolutionary and ecological significance.

Section snippets

Fish

Juvenile Pacific herring (8.2 to 13.8 g) were obtained through a local supplier in West Vancouver, BC. Fish were transported to facilities at the Fisheries and Oceans Canada, West Vancouver Laboratory, BC, with a minimal use of nets to reduce trauma to the young fish. Fish were held in 500-L fiberglass tanks supplied with flowing filtered seawater, salinity 31 ppt, water temperature 11.0 ± 0.5 °C and dissolved O2 content above 95% saturation. Following transfer, mortality in the first week was

Chemical analysis

Initial aqueous TPAH concentrations in exposure tanks were: control (0.07 to 0.24 μg/L), low (7.3 to 12.1 μg/L), medium (26.2 to 49.6 μg/L) and high (78.3 to 120.2 μg/L). TPAH concentrations declined with time, and since declines were similar across treatments, each exposure treatment remained distinct (Fig. 1). Comparable aqueous concentrations were reported by Carls et al. (1995) using a similar design. In that study, alkane concentrations ranged from 1.28 μg/L (control) to 119 μg/L with

Discussion

This study focused on the impacts of aqueous hydrocarbon exposure on an economically and ecologically important teleost, the Pacific herring, and successfully utilized a previous method for exposing fish to aqueous hydrocarbons generated from crude oil (Carls et al., 1995) in which smaller and more volatile hydrocarbons (e.g. naphthalenes) predominate initially, with larger PAHs (e.g. phenanthrenes) becoming relatively more abundant with time. This study documented the induction of

Acknowledgements

The research described here was supported by the Exxon Valdez Oil Spill Trustee Council through contracts with the Alaska Department of Fish to CJK and APF. However, the findings and conclusions presented by the authors are their own and do not necessarily reflect the view or position either agency. We greatly appreciate the analytical chemistry support provided us by the National Oceanic and Atmospheric Administration, National Marine Fisheries Service, Auke Bay Laboratory, AK. Fisheries and

References (59)

  • R.E. Thomas et al.

    Effect of water soluble fraction of Cook Inlet crude oil on swimming performance and plasma cortisol in juvenile coho salmon (Oncorhynchus kisutch)

    Comp. Biochem. Physiol., C

    (1987)
  • K. Uchida et al.

    Localization of cortisol receptor in branchial chloride cells in chum salmon fry

    Gen. Comp. Endocrinol.

    (1998)
  • S.M. Adams

    Status and use of biological indicators for evaluating the effects of stress in fish

    Am. Fish. Soc. Symp.

    (1990)
  • A.Y.A Alkindi et al.

    Endocrine, osmoregulatory, respiratory and haematological parameters in flounder exposed to the water-soluble fraction of crude oil

    J. Fish Biol.

    (1996)
  • J.W. Anderson et al.

    Characteristics of dispersions and water-soluble extracts of crude and refined oils and their toxicity to estuarine crustaceans and fish

    Mar. Biol.

    (1974)
  • M.I. Badawy et al.

    Hydrocarbons in seawater, sediment and oyster from the Omani coastal water

    Bull. Environ. Contam.

    (1991)
  • M.G. Barron et al.

    Photoenhanced toxicity of aqueous phase and chemically dispersed weathered Alaska North Slope crude oil to Pacific herring eggs and larvae

    Environ. Toxicol. Chem.

    (2003)
  • E.D. Brown et al.

    Injury to the early life history stages of Pacific herring in Prince William Sound after the Exxon Valdez oil spill

    Am. Fish Soc. Symp.

    (1996)
  • M.D. Burke et al.

    Ethoxyresorufin: direct fluorometric assay of microsomal O-dealkylation which is preferentially induced by 3-methylcolanthrene

    Drug Metab. Dispos.

    (1974)
  • M.G. Carls et al.

    The impact of adult pre-spawn herring (Clupea harengus pallasi) on subsequent progeny. Restoration project 94166 annual report. National Oceanic and Atmospheric Administration

    (1995)
  • M.G. Carls et al.

    Expression of viral hemorrhagic septicemia virus in pre-spawning Pacific herring (Clupea pallasi) exposed to weathered crude oil

    Can. J. Fish. Aquat. Sci.

    (1998)
  • M.G. Carls et al.

    Sensitivity of fish embryos to weathered crude oil: Part I. Low-level exposure during incubation causes malformations, genetic damage, and mortality in larval Pacific herring (Clupea pallasi)

    Environ. Toxicol. Chem.

    (1999)
  • L. DiMichele et al.

    Histopathological and physiological responses on Fundulus heteroclitus to naphthalene exposure

    J. Fish. Res. Board Can.

    (1978)
  • E.M. Donaldson

    Reproductive indices as measures of the effects of environmental stressors in fish

    Am. Fish. Soc. Symp.

    (1990)
  • F.R. Englehardt et al.

    Hydromineral balance and gill morphology in rainbow trout, Salmo gairdneri, acclimated to fresh and seawater, as affected by petroleum exposure

    Aquat. Toxicol.

    (1981)
  • M.M. Gagnon et al.

    EROD induction and biliary metabolite excretion following exposure to the water accommodated fraction of crude oil and to chemically dispersed crude oil

    Arch. Environ. Contam. Toxicol.

    (2000)
  • G.R. Gardner

    Chemically induced lesions in estuarine or marine teleosts

  • T. Hansson et al.

    Effects of cortisol administration on components of the hepatic microsomal mixed function oxidase system (MFO) of immature rainbow trout (Salmo gairdneri Rich.)

    Acta Pharm. Toxicol.

    (1978)
  • R.A. Heintz et al.

    Sensitivity of fish embryos to weathered crude oil: Part II. Increased mortality of pink salmon (Oncorhynchus gorbuscha) embryos incubating downstream from weathered Exxon Valdez crude oil

    Environ. Toxicol. Chem.

    (1999)
  • Cited by (76)

    • Diluted bitumen-induced alterations in aerobic capacity, swimming performance, and post-exercise recovery in juvenile sockeye salmon (Oncorhynchus nerka)

      2022, Aquatic Toxicology
      Citation Excerpt :

      Dilbit spill events point to the importance of research into the effects of dissolved low [TPAC] through a range of exposure durations on ecologically relevant physiological functions in species at risk; here, an evaluation of aerobic capacity, swim performance, and exercise recovery in sockeye salmon was performed. The passive diffuser system used generated a CLB WSFd with TPAC concentrations as reported previously (3.5-100 μg/L, Lin et al., 2020; Alderman et al., 2017a, b, 2018; Avey et al., 2020), as well as for WSFds of Alaska North Slope crude oil (ANSCO) (7.4-127.0 μg/L; Kennedy and Farrell, 2005, 2006, 2008). WSFds were initially dominated by volatile and low molecular weight hydrocarbons (e.g., BTEX, naphthalene), and high molecular weight compounds becoming relatively more prominent as exposures progress in conjunction with declining total [TPAC] (Lin et al., 2020) as is found during the normal weathering process (Alsaadi et al., 2018a; NASEM, 2016).

    • Environmental modulators of diluted bitumen effects in juvenile pink salmon (Oncorhynchus gorbuscha)

      2021, Marine Environmental Research
      Citation Excerpt :

      It is also possible that dilbit-exposed fish had lower stored glycogen and higher lactate levels before the swim test due to a higher basal glycolytic activity (e.g., phosphofructokinase, lactate dehydrogenase, creatine phosphokinase activities) or stress response. Exposure to crude oil and PAHs can initiate a physiological stress response and elevate of circulating catecholamine and cortisol levels (Hontela et al., 1992; Kennedy and Farrell, 2005), increasing the metabolism of glycogen and accumulation of lactate (George et al., 2013). Stress under WAF exposure may alter energy relocation towards fuel-intensive activities in fish, thereby negatively impacting anaerobic performance.

    View all citing articles on Scopus
    View full text