Distinguishing multiple Zn sources in oysters in a complex estuarine system using Zn isotope ratio signatures☆
Graphical abstract
Introduction
Variations in the abundance of metal isotopes increasingly have found application in many environmental studies (see Wiederhold (2015) for a review). Several factors can contribute to the metal isotope ratios measured in an environmental compartment, such as water, soil, sediments or biota. These include the contributions from a single source, or from multiple sources with different isotopic signatures and as well, changes in isotopic fractionation that might occur within the compartment (Araújo et al., 2017; Chen et al., 2008; Ma et al., 2020, 2019; Weiss et al., 2005). Understanding the variations in source signatures, mixing processes that affect multiple sources under specific environmental conditions, as well as the in vivo processes that could alter the isotope ratio in a biotic sample, is critical in employing isotope ratios in sentinel organisms to determine the sources of contamination. Moreover, finding suitable end points to use for source identification is also a valuable part of validating this method.
The Pearl River Estuary (PRE) is surrounded by mega cities in the Pearl River Delta, an important economic region of southern China and part of the Guangdong - Hong Kong - Macau Greater Bay Area. Significantly elevated levels of metal contaminants, as well as site-to-site variations in metal concentrations have previously been reported in water, sediment and biota from the PRE (Chen et al., 2012; Hong et al., 2018; Li et al., 2000a, 2000b; Lu et al., 2017; Ma et al., 2020, 2019; Ouyang et al., 2006; Xie and Wang, 2020; Yin and Wang, 2017). While there is ample evidence of metal contamination in the estuary, at present it is unknown whether it is possible to identify what sources contribute to the contamination at any given location. In addition, it is necessary to better understand metal discharge sources and their redistribution within the PRE for ultimate assessment of the environmental impact of the PRE on the South China Sea and best mitigation measures.
Bivalves such as mussels and oysters have been used widely as sentinels to monitor the temporal changes in contaminant levels in coastal areas worldwide (Phillips and Rainbow, 1994; Lu et al., 2020), and more recently metal isotope ratios also have been used to trace contamination sources. For example, Cd, Zn and Pb sources were determined using isotope ratios in oysters collected from a coastal area of BC, Canada and from the east coast of the USA (Shiel et al., 2012). Other examples include determination of Zn isotope ratios in oysters obtained from a fluvial estuarine system in France (Petit et al., 2015) and from a tropical estuary in Brazil (Araújo et al., 2017). Recently, Ma et al. (2020) analyzed Zn isotope ratios in water samples collected from 17 locations in the PRE. Their results indicated that variations in Zn isotope ratios may be related not only to water discharged from anthropogenic activities, but also to water circulation patterns in the estuary and variations in the volume of water discharged from the tributaries of the Pearl River in wet versus dry seasons. However, using only Zn isotopic compositions in water samples, they were unable to separate the influence of particles delivered to the estuary by high water discharge from the Pearl River during the wet season, from water circulation patterns and different mixing processes that can occur in wet versus dry seasons. Experimentally, using zinc exposures with distinct isotope signatures, isotope ratios in oysters have been shown to have the potential to distinguish Zn sources (Ma et al., 2019). However, this previous study used only soluble Zn as exposure sources. Soluble versus particulate sources may vary over long periods of exposure (Hall et al., 2020). Tan et al. (2018) transplanted oysters from a ‘clean’ area to a contaminated estuary for 48 days. The results, obtained from a toxicokinetic model, showed that both dissolved and particulate fractions of Zn were important pathways to the oysters and contributed equally to the Zn bioaccumulation. However, their experimental area had only a single well-known metal discharge source and the hydrological conditions were much less complex compared to the PRE (Tan et al., 2018; Weng and Wang, 2015; Xie and Wang, 2020). The uptake sources, i.e., from dissolved or particulate fractions of Zn, can be variable in oysters under different biogeochemical processes in estuarine systems (Araújo et al., 2017; Petit et al., 2015). Given the current evidence available in the literature, it is unclear whether Zn isotope ratios in oysters can distinguish between soluble and particulate exposure as well as variations in point sources of contamination.
In the present study, Zn concentrations and Zn isotope ratios were measured in the soft tissues of oysters collected from 8 locations in the PRE on four occasions (December 2014, June 2016, December 2016 and December 2018). Given that oysters can accumulate Zn from both dissolved and particulate fractions and the large variations in Zn isotope ratios previously reported in the water and suspended particles in the PRE (Ma et al., 2020), we hypothesized that Zn contributions from different sources could be identified by comparing the δ66Zn values in oysters with those in various environmental compartments. A mixing model was then developed to predict the relative contributions from multiple sources to the measured δ66Zn values in an attempt to test if Zn isotope ratios in oysters can be used for tracking sources in this complex and contaminated area.
Section snippets
Oyster collections
Crassostrea hongkongensis, a major estuarine species of oysters in the PRE, were sampled at low tide at 8 estuarine sites (E1, E2, E3, E4, W1, W2, W3, W4, Fig. 1) in December 2014, June 2016, December 2016, and December 2018. Significant differences in hydrological conditions as well as the levels of metal contamination have been reported among the 8 locations (Lu et al., 2020; Ma et al., 2020; Xie and Wang, 2020). Oysters were collected during the dry season (i.e., December) every two years
Total Zn concentrations and δ66Zn values in oysters
Zn concentrations in the oysters collected from the PRE varied from 2070–5322 μg g−1 (dry weight) in December 2014, 1387–10,767 μg g−1 in June 2016, 3163–10,561 μg g−1 in December 2016, and 181–13,479 μg g−1 in December 2018 (Fig. 2), respectively. The slight increase in Zn concentrations in the oysters over the 4-year sampling period could be caused by changes to anthropogenic inputs to the PRE (Lu et al., 2020; Ma et al., 2020). Lower concentrations were seen overall in oysters collected from
Author contribution statement
Lan Ma: Conceptualization, Investigation, Writing; Doug Evans: Conceptualization, Writing. Wen-Xiong Wang: Conceptualization, Writing.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank Drs. Guangyuan Lu, Nanyan Weng, Chunlian Lai, Yunlong Li for their help with sample collection. This research was funded by a NSERC Canada (Natural Sciences and Engineering Research Council) Discovery Grant to R.D.E., the Natural Science Foundation of China (21777134), the General Research Fund of Hong Kong Research Grants Council (CityU 16102918), and the TUYF fund (19SC01) to W.X.W. Hayla Evans helped to revise the manuscript.
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This paper has been recommended for acceptance by Philip N. Smith.