Elsevier

Aquatic Toxicology

Volume 96, Issue 3, 18 February 2010, Pages 203-215
Aquatic Toxicology

Evidence for thyroid endocrine disruption in wild fish in San Francisco Bay, California, USA. Relationships to contaminant exposures

https://doi.org/10.1016/j.aquatox.2009.10.023Get rights and content

Abstract

It is well documented that many coastal and estuarine environments adjacent to developed and industrialized urban centers, such as the San Francisco Bay Area, are significantly contaminated by anthropogenic chemicals. However, it is not well understood to what extent existing contaminants, many with continuing inflows into the environment, may impact exposed wildlife. This study provided an initial characterization of thyroid endocrine-related effects and their relationship to accumulated contaminants in two indigenous fish species sampled from different San Franicsco Bay Area study sites. Plasma concentrations of thyroxine (T4) were significantly reduced in fish sampled from highly impacted locations such as Oakland Inner Harbor and San Leandro Bay as compared with fish from other locations representing relatively lower human impact, including Bodega Bay, Redwood City and a remote site on Santa Catalina Island. Triiodothyronine (T3) levels also varied significantly by location, with differing T3/T4 ratios in fish from some locations suggestive of altered peripheral deiodinase activity. The changes in thyroid endocrine parameters were significantly correlated with hepatic concentrations of certain environmental contaminants. A large number of polychlorinated biphenyl (PCB) congeners, both co-planar (dioxin-like) and non-co-planar, exhibited significant inverse correlations with T4 levels in the fish, while in contrast, T3 and T3/T4 ratio were positively correlated with PCB exposures. The positive correlation between T3/T4 ratio and PCBs supports the hypothesis that environmental PCBs may alter T4 deiodination or turnover, actions of PCBs reported in laboratory experiments. Some relationships between chlorinated pesticides including DDT and chlordanes, but fewer relationships with PAHs, were also observed. Together, these findings indicate that the thyroid endocrine system is exhibiting alterations associated with different aquatic environments in the San Francisco Bay Area, which are significantly related to current-day exposures of the fish to contaminant chemicals such as PCBs.

Introduction

In aquatic environments adjacent to large urban centers, such as in the San Francisco Bay Area, a wide variety of chemical contaminants are typically present, yet their phenotypic effects in resident fish and other wildlife are not well understood. Selected chemicals which can be present in such environments may have thyroid-disrupting effects in fish, as indicated from laboratory experiments. Since thyroid hormones have critical roles in development and physiological homeostasis, disruption of the thyroid system can present a threat to health in wild fish populations. However, studies are lacking that evaluate, within a real ecosystem, the connections between altered endocrine phenotype and environmental contaminant exposures.

Thyroid hormones are produced upon activation of the neuroendocrine hypothalamo-pituitary-thyroid (HPT) axis (reviews by Eales, 2006, Blanton and Specker, 2007, Zoeller et al., 2007). Under hypothalamic control, the pituitary secretes thyroid-stimulating hormone (TSH) which proceeds to the thyroid gland to activate synthesis of thyroxine (T4; 3,5,3′,5′-tetraiodo-l-thyronine) and triiodothyronine (T3; 3,5,3′-triiodo-l-thyroinine). T4 generally represents >95% of the thyroid hormone output and it is typically present in higher quantities than T3 in the blood circulation, with the higher T4 concentrations serving as a pool of prohormone that can be converted into T3 by 5′-iodothyronine deiodinases in target tissues (Eales, 2006, Zoeller et al., 2007). Thyroid hormones are essential for early development in fishes, including larval–juvenile transitions and induction of metamorphosis in flatfish (Inui et al., 1995, Power et al., 2001, Yamano, 2005, Shiao and Wang, 2006, Blanton and Specker, 2007, Klaren et al., 2008). Thyroid hormones are also deposited into the yolk of fish eggs, and used during subsequent embryonic development (Kobuke et al., 1987, Leatherland, 1989). In juvenile and adult life, they are necessary (permissive) for normal somatic growth and have a number of effects on growth endocrine genes, such as pituitary growth hormone (GH), GH receptors, and insulin-like growth factor-I (IGF-I; Power et al., 2001, Plohman et al., 2002, Schmid et al., 2003).

Given the multi-component neuroendocrine HPT axis, there are a large number of potential target genes or proteins that can be altered by endocrine-disrupting chemicals (EDCs). Such effects may range from agonistic to antagonistic actions of EDCs on target tissue receptors, to alterations in thyroid hormone synthetic pathways, deiodinase functions in peripheral tissues, or carrying proteins in the blood (Brown et al., 2004a, Boas et al., 2006, LeRoy et al., 2006, Zoeller, 2007, Crofton, 2008, Soldin et al., 2008). Polychlorinated biphenyls (PCBs), dioxin (2,3,7,8-tetrachlorodibenzo-p-dioxin; TCDD), chlorinated pesticides, polybrominated diphenyl ethers (PBDEs), and metals such as mercury, have all been implicated as thyroid-disruptive agents when tested experimentally in fish (Adams et al., 2000, Brown et al., 2004a, Brown et al., 2004b, Boas et al., 2006, Kahn et al., 2002, LeRoy et al., 2006, Soldin et al., 2008). However, current knowledge is limited mostly to laboratory testing of a small subset of chemicals that are found within human-impacted environments.

The San Francisco Bay appears on the “Section 303(d) list” of impaired water bodies, as required by the federal Clean Water Act. The California State Water Board compiled the most recent 303(d) list in 2006, approved by the US EPA in 2007 (http://www.waterboards.ca.gov/sanfranciscobay/TMDL/303dlist.htm). Contaminants in San Francisco Bay and its major tributaries on this 303(d) list include polyaromatic hydrocarbons (PAHs), pesticides (dieldrin, chlordanes, and DDTs), additional chlorinated compounds such as PCBs, TCDD, furan compounds, and trace elements (Hg and Se). Total maximum daily loads (TMDLs), required of water bodies on the 303(d) list, have been developed for PCBs, Hg, Cu and Ni (adopted in 2008) or are currently in development (for pesticides, TCDD, others).

Contaminants such as PCBs and pesticides accumulate to high concentrations at the top of the food web and therefore may pose a health risk to piscivorous and other wildlife. The Regional Monitoring Program for Water Quality in the San Francisco Estuary (RMP; http://www.sfei.org/rmp) has monitored contaminant concentrations in sport fish every three years since 1997. Data collected by the RMP series and in other studies indicate that contaminant concentrations in the San Francisco Bay ecosystem are sufficiently elevated to cause concern for adverse effects on biota (Fairey et al., 1997, Davis et al., 2004, Davis et al., 2007, Greenfield et al., 2005, Oros et al., 2005, Oros et al., 2007, San Francisco Estuary Institute, 2008). In the 2003 and 2006 RMP fish contamination surveys, several fish species were demonstrated to have tissue concentrations of total PCBs (sum of congeners) of 100–200 ng/g wet weight (ww) or higher, as compared with a screening value of 10 ng/g ww (PCB TMDL of the San Francisco Bay Regional Water Quality Control Board). Given sediment PCB concentrations between 5.7 and 8.7 ppb in recent years (San Francisco Estuary Institute, 2008), substantial bioaccumulation into fish tissues is indicated. In addition to PCBs, several other contaminants are present in fish tissues at concentrations above thresholds of concern, including pesticides, Hg, dioxin, and PBDEs (Fairey et al., 1997, Davis et al., 2004, Greenfield et al., 2005, Oros et al., 2005, Oros et al., 2007). The potential for endocrine disruptive effects and other phenotypic/physiological effects due to exposure to these contaminants are not well understood.

In California and elsewhere, water quality objectives and management of coastal and estuarine environments have been based largely upon contaminant concentrations, with little additional information on biological effects in resident wildlife. This study therefore pursued establishing linkages between contaminant exposures and effects in a critical endocrine system, as a first step toward understanding phenotypic impacts of existing contaminants. We evaluated the hypothesis that current-day exposures to environmental contaminants in San Francisco Bay Area aquatic habitats can be related to indices of thyroid endocrine status in resident wild fish. In addition, it was of interest to determine whether differences in thyroid status could be differentiated among study sites that represented differing signatures of contaminant chemicals.

Section snippets

Study fish

The target fish species included shiner surfperch (Cymatogaster aggregata) and Pacific staghorn sculpin (Leptocottus armatus), both indigenous to San Francisco Bay. The shiner surfperch has received continuing monitoring for tissue contaminant levels by the RMP since 1997 (http://www.SFEI.org/rmp). Pacific staghorn sculpin is typically captured at the same locations as the surfperch and exhibits strong site fidelity during its first year, remaining mostly along the Bay margins and in

Animals

For surfperch, overall mean body lengths were 9.5 ± 0.4 cm in 2006 and 9.1 ± 0.1 cm in 2007, which were not significantly different between years. In addition, there were no significant differences in mean body length among groups (study locations) in 2006. In 2007, most groups were also not significantly different in length, except that the OAK (9.6 ± 0.2 cm) and CAT (9.9 ± 0.2 cm) groups had slightly higher means than the RCH (8.5 ± 0.2 cm) and TOB (8.5 ± 0.15 cm) groups (p < 0.05). Based upon available length

Discussion

The findings of the present study and several former studies (Fairey et al., 1997, Davis et al., 2004, Davis et al., 2007, Oros et al., 2005, Oros et al., 2007, Hunt et al., 2008) have consistently demonstrated that wild fish residing in San Francisco Bay Area habitats are exposed to a variety of anthropogenic contaminants. It has not been well understood, however, the extent to which such contaminant exposures may be related to phenotypic effects. This study provided an initial

Conclusion

In conclusion, this study identified significant alterations in the thyroid endocrine system of two fish species in association with different environments in the San Francisco Bay Area. Several of the alterations were consistent between the species as well as between two years of study. Differing patterns of response in thyroid endocrine parameters suggested more than one underlying mechanism of effect. Exposure to PCBs appears to be at least one possible cause of the thyroidal alterations,

Conflict of interest

The authors declare that no conflict of interest exists that would prejudice the impartiality of this scientific work.

Acknowledgments

This work was supported by the Regional Monitoring Program for Water Quality in the San Francisco Estuary, through the Exposure and Effects Pilot Studies (EEPS) Workgroup at the San Francisco Estuary Institute (http://www.SFEI.org/rmp) and the Pacific Coast Environmental Conservancy (http://www.PCEConservancy.org). We thank the following persons for their valued contributions to the work described in this report: Rich Gossett (CRG Laboratories, Torrance, CA) and A. Zed Mason (California State

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