Spatial and temporal variability of contaminants within estuarine sediments and native Olympia oysters: A contrast between a developed and an undeveloped estuary
Graphical abstract
Introduction
Estuarine and marine ecosystems provide the foundation for an invaluable suite of ecosystem services, including provisioning, regulating, supporting, and cultural benefits (MEA, Millenium Ecosystem Assessment, 2005). Over 50% of the global population currently resides within 80 km of the coast, and ocean ecosystems are now recognized to simultaneously be of great importance and under increased pressure from human populations worldwide (UNEP, 2006). Pollutants including persistent legacy contaminants and those of emerging concern present an ongoing threat to marine ecosystems, and they have the potential to damage and degrade a variety of ecosystem benefits as well as pose a risk to human health (e.g., Fleming et al., 2006, Kimbrough et al., 2008). Persistent legacy contaminants such as dichlorodiphenyltrichloroethane (DDT) and polychlorinated biphenyls (PCBs) remain in the environment long after they are introduced and several congeners are potentially carcinogenic to humans and animals. Contaminants of emerging concern (CECs) include pharmaceuticals, natural and synthetic hormones, and chemicals in personal care products that, historically, had less data available, but which, in recent years, have been recognized as potentially serious environmental threats, particularly to the endocrine and reproductive systems (Glassmeyer et al., 2005). For example, the sex ratio of white sucker fish (Catostomus commersonii) was biased toward females and a large proportion of intersex fish was observed downstream of wastewater treatment plant effluent that contained a mixture of hormones and hormone-mimicking surfactant metabolites (Vajda et al., 2008). Chronic exposure of a lake population of fathead minnow (Pimephales promelas) to low concentrations (5–6 ng/L) of the potent synthetic estrogen 17α-ethynylestradiol led to feminization of males, altered oogenesis in females, and ultimately, a near extinction of this species from the lake (Kidd et al., 2007).
Persistent contaminants and CECs may be introduced into the environment from a variety of sources. For example, although commercial use of PCBs is largely prohibited in the US, several uses are still authorized including incorporation into electrical and railroad transformers, natural gas pipelines, circuit breakers, and carbonless copy paper, and other applications (Oregon Department of Environmental Quality, ODEQ, 2003). Agricultural lands are an ongoing source of pesticides and herbicides, such as DDT and its breakdown products (dichlorodiphenyldichloroethane [DDD] and dichlorophenyldichloroethylene [DDE]), dieldrin, and chlordane. Household waste and dust are sources of polybrominated diphenyl ether (PBDE) flame retardants, which are used in motor vehicles, electronics and furniture (Schreder and La Guardia, 2014). Dioxins and furans are by-products emitted from a variety of industrial activities. Metals such as mercury may be transported to water bodies during wet deposition and overland runoff. Pharmaceuticals and personal care products (PPCPs) are discharged into the environment from households, hospitals, health-care facilities and other commercial operations. Consumers can excrete prescription or non-prescription pharmaceuticals at low concentrations, and excess pharmaceuticals are often flushed down the drain. Compounds in personal care products, such as alkylphenol-based surfactant metabolites present in soaps and detergents, are also washed away in sinks, showers, and lavatories. Consequently, wastewater treatment systems and onsite waste (i.e., septic) systems provide pathways of entry for these compounds into freshwater and marine systems (e.g., Paul et al., 1997, Conn et al., 2010). Several pharmaceuticals are also used to raise livestock; these compounds may be excreted by livestock and carried into rivers and streams (Barnes et al., 2002).
Little information is available on the occurrence of CECs and other contaminants in ecologically-sensitive areas such as estuarine and marine waters. Recent studies in Oregon revealed the presence of several different types of contaminants in the Willamette and Columbia Rivers which drain to the Oregon coast, within the Coos Estuary on the Oregon coast, and in wastewater effluent discharged into these waterbodies (Fig. 1; Hope et al., 2012, Morace, 2012, Nilsen et al., 2014, Pillsbury et al., 2015). However, very little information exists about contaminant concentrations in marine and estuarine organisms that occur in regions where the human population is low (i.e., less than 100,000 people along the entire Oregon coast). Historical sampling of marine organisms by the National Oceanographic and Atmospheric Administration (NOAA) Mussel Watch Program included mussel (Mytilus spp.) samples from six sites along the Oregon coast. This long term monitoring did not include CECs or Olympia oysters (Ostrea lurida; Kimbrough et al., 2008). Other coastal monitoring efforts such as EPA's National Coastal Condition Assessment do not include bivalves, which are important foundation species that filter feed and thereby accumulate chemical compounds. In the 1990s, sampling of softshell clams, oysters, and Dungeness crab in Coos Bay detected contaminants including butyltins and metals (ODEQ, personal communication).
Since exposure to multiple CECs with different modes of action may be a coast-wide ecological problem and potential human health issue, we examined the types and concentrations of contaminants and spatio-temporal variability of those compounds in two Oregon estuaries. Accumulation of persistent compounds and CECs in marine life has implications for ecological community structure, recreational and tribal shellfishing, and potential health consequences for human consumers (Guéguen et al., 2011, Gaw et al., 2014). The native Olympia oyster, the target species for this study, has drastically declined in abundance and distribution along the Pacific coast since the mid-1800s (White et al., 2009). In Oregon, several groups including NOAA, the South Slough National Estuarine Research Reserve, the Oregon Department of Fish and Wildlife, and The Nature Conservancy recently initiated actions to facilitate and guide restoration of Olympia oysters (Rumrill, 2010, Wasson et al., 2015). Recent sampling to examine CEC levels in Dungeness crabs (Cancer magister), California mussels (Mytilus californianus), and Oregon's coastal environment detected a suite of persistent legacy contaminants and CECs (Rodriguez del Rey, 2010; Granek, unpublished data).
Here we present new information about the chemical compounds and contaminant concentrations in sediment and oyster tissues from two Oregon estuaries that differ in the level of municipal, residential and industrial development. Our specific hypothesis is that persistent legacy contaminants and CECs will be elevated in sediments and oysters sampled from Coos Bay where municipal and residential development is extensive. Although moderate in urbanization compared to other U.S. estuaries, Coos Bay is considered urban is comparison to other Oregon estuaries. In contrast, we anticipate that contaminant levels will be low in Netarts Bay where residential development is much lower and industrial operations are non-existent. Both sites are inhabited by significant and recovering populations of native Olympia oysters. We also expect that seasonal variability (e.g., from precipitation) and spatial variability (e.g., from land-use practices and population density) contribute to variability in the concentrations of environmental contaminants observed in the estuarine sediments and oyster tissues.
Section snippets
Study sites
Olympia oysters (Ostrea lurida) were historically abundant but have been lost from much of their native range along the US West Coast (Beck et al., 2011). In Oregon, populations persist in Coos Bay, Yaquina Bay, and Netarts Bay where native oyster restoration efforts and commercial shellfish operations have helped enhance the populations. We focused our sampling within Coos Bay and Netarts Bay (Fig. 1, Table 1) where sufficient numbers of Olympia oysters can be collected without harm to the
Oyster tissue
Chemical detections and concentrations varied by estuary, time period and compound category. All of the compound groups, with the exception of dioxins/furans, were detected in oyster tissue during at least one season (Table 4, Table 5). Of the CECs, three (of 4 tested) alkylphenols and five (of 59) PPCPs were detected. The pharmaceuticals detected included antibiotics, an antihistamine, and an anti-inflammatory substance (Table 4). One (of 4) heavy metals (mercury) and 13 (of 69) pesticides,
Discussion
Contaminant types and concentrations in Olympia oysters and sediments differed substantially between Netarts and Coos Bays, at the sample locations studied (Fig. 2, Table 4, Table 5, Table 6). Considering all detections, PPCPs were detected more frequently in the samples collected from Coos Bay; surprisingly, compounds that were detected within both estuaries (alkylphenols) occurred at similar concentrations (Table 4). We observed relatively large differences in oyster tissue concentrations of
Acknowledgements
This work was made possible through funding from Oregon Sea Grant in the form of Program Development Grant #NA154C-A to EFG; Contaminants Grant #NA10OAR4170059 to EFG, ALS, WF, KEC, EBN, LP, SSR and through funding from the Oregon Community Foundation in the form of an Oregon University System Katherine Bisbee II Grant to EFG and AMF. We thank Oregon Sea Grant and the Oregon Community Foundation for their support. We thank ODEQ Laboratory for analytical support and Tony D'Andrea and ODFW staff
References (39)
- et al.
Oceans and human health: emerging public health risks in the marine environment
Mar. Pollut. Bull.
(2006) - et al.
Uptake and depuration of toxic halogenated aromatic hydrocarbons by the American oyster (Crassostrea virginica): a field study
Chemosphere
(2004) Centers for disease control and prevention
- et al.
A state-wide survey in Oregon (USA) of trace metals and organic chemicals in municipal effluent
Sci. Total Environ.
(2012) - et al.
Contaminants of emerging concern in a large temperate estuary
Environ. Pollut.
(2016) - et al.
Contaminants of legacy and emerging concern in largescale sucker (Catostomus macrocheilus) and the foodweb in the lower Columbia River, Oregon and Washington, USA
Sci. Total Environ.
(2014) - et al.
Evidence for groundwater and surface marine water contamination by waste disposal wells in the Florida keys
Water Res.
(1997) - et al.
Accumulation and depuration of organic contaminants by the American oyster (Crassostrea virginica)
Sci. Total Environ.
(1996) - et al.
Indicators of sediment and biotic mercury contamination in a southern New England estuary
Mar. Pollut. Bull.
(2012) - et al.
Water-quality Data for Pharmaceuticals, Hormones, and Other Organic Wastewater Contaminants in U.S. Streams, 1999–2000
(2002)
Oyster reefs at risk and recommendations for conservation, restoration, and management
Bioscience
Fate of trace organic compounds during vadose zone soil treatment in an onsite wastewater system
Environ. Toxicol. Chem.
R: A Language and Environment for Statistical Computing
One-year monitoring survey of organic compounds (PAHs, PCBs, TBT), heavy metals and biomarkers in blue mussels from the Arcachon bay, France
J. Environ. Monit.
Bioaccumulation and distribution of heavy metals (Cd, Cu, Fe, Ni, Pb and Zn) in the different tissues of Chicoreus capucinus Lamarck (Mollusca: Muricidae) collected from Sungai Janggut, Kuala Langat, Malaysia
Environ. Asia
Sources, impacts and trends of pharmaceuticals in the marine and coastal environment
Philos. Trans. R. Soc. B
Transport of chemical and microbial compounds from known wastewater discharges: potential for use as indicators of human fecal contamination
Environ. Sci. Technol.
Shellfish and residual chemical contaminants: hazards, monitoring, and health risk assessment along French coasts
Rev. Environ. Contam. Toxicol.
Collapse of a fish population after exposure to a synthetic estrogen
PNAS
Cited by (21)
Seasonal profile of common pharmaceuticals in edible bivalve molluscs
2024, Marine Pollution BulletinAntibiotics in the marine environment: occurrence and impact
2023, Contaminants of Emerging Concern in the Marine Environment: Current Challenges in Marine PollutionPresence of pharmaceuticals and their metabolites in wild-living aquatic organisms – Current state of knowledge
2022, Journal of Hazardous MaterialsCitation Excerpt :Marine waters were neglected for a long time because it was assumed that “the solution to pollution is dilution” thus final dilution of the effluent neglected the risk of pharmaceutical residues leaking into the environment (Fabbri and Franzellitti, 2016). However, recent years have seen a marked increase in research on saltwater and thus on the organisms living in it (Fig. 1) (Li et al., 2012; Granek et al., 2016; Meador et al., 2016; Mezzelani et al., 2020). The number of publications describing concentration of pharmaceuticals in plants and animals is relatively low compared to the number of publications dealing with analysis of pharmaceuticals in water media.
Variability of trace metals in coastal and estuary: Distribution, profile, and drivers
2022, Marine Pollution BulletinCitation Excerpt :Moreover, assessment of the pollution load index shows that the quality of the sediment deteriorates during the pre-monsoon season (Satapathy and Panda, 2015). Research conducted by Granek et al. (2016) shows that the concentration of sedimentary trace metals in Coos Bay is higher than in Netarts Bay, with spatial variability estimated to be influenced by land-use practices and population density. In addition, for areas inhabited by residents relying on agricultural activities, the potential source of trace metals in sediments is the use of excessive fertilizers and pesticides that flow into the sea through irrigation.
Pharmaceuticals and alkylphenols in transplanted Pacific oysters (Crassostrea gigas): Spatial variation and growth effects
2021, Marine Pollution BulletinAnalysis of the occurrence of microplastics in beach sand on the Brazilian coast
2021, Science of the Total Environment