Historical biomonitoring of pollution trends in the North Pacific using archived samples from the Continuous Plankton Recorder Survey

https://doi.org/10.1016/j.scitotenv.2022.161222Get rights and content

Highlights

  • This study reports the use of archived plankton samples for ocean pollution monitoring.

  • Samples from the Continuous Plankton Recorder (CPR) Survey were analyzed.

  • Dozens of anthropogenic chemicals displayed distinct spatiotemporal trends.

  • Phthalates from personal care products and plastics increased from 2002 to 2020.

  • Plankton nearest to human population centers had more complex exposomes.

Abstract

First started in 1931, the Continuous Plankton Recorder (CPR) Survey is the longest-running and most geographically extensive marine plankton sampling program in the world. This pilot study investigates the feasibility of biomonitoring the spatiotemporal trends of marine pollution using archived CPR samples from the North Pacific. We selected specimens collected from three different locations (British Columbia Shelf, Northern Gulf of Alaska, and Aleutian Shelf) in the North Pacific between 2002 and 2020. Comprehensive profiling of the plankton chemical exposome was conducted using liquid and gas chromatography coupled with tandem mass spectrometry (LC-MS/MS and GC–MS/MS). Our results show that phthalates, plasticizers, persistent organic pollutants (POPs), pesticides, pharmaceuticals, and personal care products were present in the plankton exposome, and that many of these pollutants have decreased in amount over the last two decades, which was most pronounced for tri-n-butyl phosphate. In addition, the plankton exposome differed significantly by regional human activities, with the most polluted samples coming from the nearshore area. Exposome-wide association analysis revealed that bioaccumulation of environmental pollutants was highly correlated with the biomass of different plankton taxa. Overall, this study demonstrates that exposomic analysis of archived samples from the CPR Survey is effective for long-term biomonitoring of the spatial and temporal trends of environmental pollutants in the marine environment.

Introduction

Marine habitats have been under increasing threat due to the intensification of coastal human activities and the growing human population around the world. The release of anthropogenic chemicals, pesticides, and fertilizers has adverse impacts on marine ecosystems (Feng et al., 2022; John et al., 2022; Martinez-Varela et al., 2021). Therefore, in addition to reducing pollutant flows into oceans, it is essential to map and monitor ocean pollution to prioritize corrective measures, assess mitigation efforts for effectiveness and ensure a healthy and productive marine environment.

While a large body of data is available on the concentrations of many anthropogenic compounds in surface waters (Cunha et al., 2022; Sanganyado et al., 2021; Wilkinson et al., 2022), substantial gaps exist in our knowledge of the temporal changes of such exposures over decades. Long-term monitoring is an important approach for assessing the fate of contaminants in marine ecosystems. It can provide a first warning of the increase of potentially toxic compounds in the environment. In addition, multi-year temporal trend analysis may indicate whether regulatory actions aimed at reducing harmful chemicals in the oceans are proving successful. Long-term monitoring of persistent organic pollutants (POPs) in the marine environment has been established using Arctic marine biota (Riget et al., 2019), seabird eggs from the East Sea (Jang et al., 2022), and dolphins in the South Atlantic Ocean (de Oliveira-Ferreira et al., 2022).

Marine plankton, found in all ocean ecosystems, form complex communities of interacting organisms at the base of the food web and play essential roles in maintaining the health and balance of the ocean and influencing climate regulation (Field et al., 1998). Most planktonic species are short-lived and sensitive to environmental changes (Batten et al., 2022; Chaffron et al., 2021; Henson et al., 2021). Therefore, plankton may be an excellent bioindicator of contamination. Started in 1931, the Continuous Plankton Recorder (CPR) Survey is the longest-running and most geographically extensive marine plankton sampling program in the world (Richardson et al., 2006). Uniquely, CPR sampling has remained unchanged in terms of mesh size, weave, and fiber, throughout the Survey's history, making the archived CPR samples standardized candidates for long-term biomonitoring of marine pollution (Batten et al., 2019; Batten et al., 2003). For xenobiotics in marine plankton, information is typically only available for a small number of chemicals such as poly- and perfluoroalkyl substances (PFAS) (Zhang et al., 2019), Tetrabromobisphenol-A (Gong et al., 2021), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs) (Peltonen et al., 2014). There is still a lack of comprehensive profiling of plankton chemical exposomes in the world's oceans.

Here, we selected archived plankton samples collected in three different locations in the North Pacific Ocean from 2002 to 2020. We quantified >1000 commonly used anthropogenic chemicals in plankton exposome using a broad-spectrum targeted approach. The targeted compounds were selected based on known occurrence in coastal marine environments and potential for biological impact. The objectives of this study were to (1) assess the temporal trends of the plankton chemical exposome in the North Pacific coastal environments over the last two decades; (2) compare the regional differences of the plankton exposome; (3) correlate the bioaccumulation of environmental pollutants within plankton with the biomass data of different plankton taxa and other ecological variables (Marine fishes abundance and GDP for agriculture, fishing, and hunting).

Section snippets

CPR Survey apparatus and collection

The samples used in this study were collected by the Continuous Plankton Recorder (CPR) Survey, the longest, multi-decadal plankton monitoring program in the world. Detailed descriptions of the CPR device and its sampling characteristics over the lifespan of the Survey can be found online (https://www.cprsurvey.org/) and in the previous publication (Richardson et al., 2006). The CPR is a mechanical device that weighs about 85 kg and measures 106 cm × 43 cm × 37 cm. It is towed behind commercial

CPR survey site selection

This study included sampling sites in the North Pacific Ocean subject to a broad suite of anthropogenic influences, spanning from the British Columbia Shelf (BC Shelf) near Vancouver, one of the most populated cities in Canada, to the Northern Gulf of Alaska (N Gulf Alaska), an ecologically productive area of the North Pacific (Fig. 1A). A site on the Aleutian Shelf was also selected, which is the home to some of the largest commercial fisheries in the United States but has a low local human

Discussion

The North Pacific region features coastal and island ecosystems with spectacular marine life and commercially important fishing resources. Rapid coastal development, onshore and offshore industry, and tourism are taking an increasing toll on the North Pacific marine and coastal environmental health (Chen et al., 2018). Even though the existing untargeted methods of exposomic analysis are capable of capturing thousands of chemical features using high-resolution mass spectrometry (HRMS), fewer

Funding

The Pacific CPR Survey is funded via a consortium of funders through the North Pacific Marine Science Organization (PICES) and comprising the North Pacific Research Board (NPRB), Exxon Valdez Oil Spill Trustee Council through Gulf Watch Alaska, Canadian Department of Fisheries and Oceans (DFO), and the Marine Biological Association. Exposome profiling and data analysis were supported in part by the UCSD Christini Fund, and the Lennox Foundation. Funding organizations had no role in the study

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.

Acknowledgments

The authors thank Douglas Moore for excellent technical assistance.

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