Recent studies have found evidence of xenoestrogenic endocrine disruption in fish from estuarine and marine environments, distant from contaminant discharges 1–3. For example, male flatfish from offshore waters of the United Kingdom contain elevated levels of the egg yolk precursor protein vitellogenin (VTG) 2. These fish responses may be the result of low-level exposure to endocrine disrupting compounds, perhaps as a result of accumulation through the food chain. Previous studies have not identified specific causal compounds and multiple contaminants of emerging concern (CECs) may play a role.
Municipal wastewater effluents are thought to be one of the main sources of CECs in aquatic environments. Contaminants of emerging concern represent a diverse range of compounds, including pharmaceuticals, personal care products, pesticides, and industrial and commercial compounds, several of which have endocrine disrupting potential. In spite of an increasing number of studies investigating CECs in aquatic systems 4, their occurrence and effects in marine ecosystems are poorly understood. Exposure to some CECs, such as pharmaceuticals and plasticizers, can lead to endocrine disruption and other physiological effects in fish, and have the potential to adversely impact fish populations and communities 5.
The coastal waters off of southern California, known as the Southern California Bight, provide a unique and challenging opportunity to investigate the impacts of CECs on the marine ecosystem. More than one billion gallons of treated municipal wastewater effluent are discharged daily into the Southern California Bight through several large ocean outfalls 6. Previous studies reported the presence of endocrine disruption indicators in fish collected near some of these outfalls 7, prompting concern regarding the impacts of unmonitored CECs. However, historical contamination of the Southern California Bight by other chemicals with endocrine disrupting potential (e.g., dichlorodiphenyltrichloroethanes [DDTs] and polychlorinated biphenyls [PCBs]) may be a contributing factor. Long-term environmental monitoring programs in this region provide information on status and trends in contamination and fish populations, essential to interpreting the ecological significance of molecular and physiological measurements.
A collaborative research program was established in 2006 among major southern California wastewater treatment agencies, academic researchers, and the Southern California Coastal Water Research Project to investigate linkages between CEC exposure, endocrine disruption, and population responses in fish in the Southern California Bight. The research program included the following three studies over a one-year period 8: (1) CECs in effluent, seawater, sediment, and tissue; (2) spatial distribution of biological responses; and (3) temporal patterns in reproductive condition. The results of this study comprise one of the most comprehensive investigations to date of CEC fate and effects in the marine environment, and were presented in a special symposium during the 2008 SETAC Annual Meeting in Tampa, Florida, USA. The papers presented in this special section describe the results of the study and address the following questions: (1) What types of CECs are discharged into the Southern California Bight from municipal wastewater outfalls? (2) Are Southern California Bight marine life exposed to CECs from municipal wastewater discharges? (3) Is there evidence of endocrine disruption or other physiological effects in Southern California Bight fish? (4) Are effects on fish related to historical or current municipal wastewater discharges? (5) Are specific chemicals responsible for the effects? (6) Are the biological effects adversely impacting fish populations?
The composition of CECs in wastewater effluents and seawater from the discharge sites was investigated by Vidal-Dorsch et al 9. The CECs most frequently detected and observed at highest concentrations in effluents were pharmaceuticals and personal care products, as well as industrial compounds like flame retardants. Some CECs were detected in seawater, although at lower concentrations than in effluent. Concentrations of CECs in seawater samples reflected the high initial dilution that the effluents undergo on discharge. The fate of CECs in sediments and fish in the Southern California Bight was described by Maruya et al 10. Several CECs were detected in sediment and livers of hornyhead turbot (Pleuronichthys verticalis). Antibacterial products, surfactants, and plasticizers were detected in all sediment samples, and flame retardants were frequently detected in fish livers. The accumulation of flame retardants in fish livers was comparable to that of DDTs and PCBs at some sites, whereas other CECs such as antibacterial products exhibited low bioaccumulation.
The reproductive endocrine status of hornyhead turbot was investigated by Reyes et al 11. Seasonal changes in sex steroids characteristic of a summer spawning season were present in fish from most sites. Differences in hormone concentrations were found between sites. Males also had relatively high concentrations of estradiol (similar or higher than females) throughout the year. However, the reproductive hormone differences were not specific to the discharge sites. Forsgren et al. 12 observed biological responses suggestive of endocrine disruption in hornyhead turbot from all sites, including the reference site. Plasma VTG was frequently detected in male fish at all sites, suggesting a widespread low-level exposure to xenoestrogenic compounds, or a species-specific normal condition. The presence of VTG in male fish did not appear to impact reproductive function, as no gonad abnormalities were observed. In general, proximity to the outfalls did not seem to alter the fish reproductive cycle or abundance.
A synthesis of the study results was conducted by Bay et al 13. Fish in the Southern California Bight are exposed to CECs from multiple sources, including the large municipal wastewater discharges, which were the focus of the study. Two patterns of biological response were evident from the hormone and VTG data, suggesting that multiple factors are important. There were widespread occurrences of VTG and elevated estradiol in males, and evidence of a diminished ability to respond to stress, indicative of biological responses throughout the entire Southern California Bight. In addition, there were reductions in estradiol and thyroxine concentrations in both males and females that indicated an association with specific wastewater discharge sites. These indications of endocrine disruption were not linked to higher level responses in hornyhead turbot, either in terms of gonad condition, reproductive cycles, or populations. The causes of these responses remain to be determined and are the subject of current research, including studies on genomic and hormonal responses following laboratory exposure to wastewater effluents. Historical contamination by organochlorine compounds and other contaminants are present throughout the Southern California Bight and a likely contributor to these effects, confounding a determination of the impacts associated with CECs in current wastewater discharges.
Field surveys such as the 2006 Coastal Effects Study in the Southern California Bight are an essential component to assessing the ecological risk posed by CECs in marine ecosystems. These ecosystems have complex food webs and multiple sources of CECs that are difficult to represent in laboratory studies, resulting in the potential that important responses or interactions will not be detected. The number of potentially harmful chemicals discharged daily into aquatic systems far exceeds our ability to chemically monitor them on an individual basis, much less evaluate their interactions and overall ecological risk in a complex environment. Multidisciplinary and collaborative field studies help overcome this challenge by providing an assessment of combined impacts under environmentally realistic exposure conditions that can be used to address environmental management questions (e.g., reproduction and population status) as well as identifying specific modes of response (e.g., estradiol synthesis/metabolism) that can be used to guide future laboratory and contaminant-specific studies.
The challenges of conducting large-scale field studies of biological responses are substantial, including sampling difficulties, uncertainty and variability associated with fish movement and biological variation, and often a lack of basic life history information or baseline data. The collaborative approach used in the 2006 Coastal Effects Study is an effective way to reduce some of these challenges. The partnership that was established between research and monitoring agencies greatly increased sampling success and provided the ability to link the individual-based measurements of physiological response to population and community condition through data from long-term monitoring programs. Future advances in technology, especially for genomic analyses and analysis of CECs in complex environmental matrices should further enhance the value of large-scale field studies for evaluating the risk of CECs in marine ecosystems.