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Environmental Modeling
Partitioning and bioaccumulation of legacy and emerging hydrophobic organic chemicals in mangrove ecosystems. Stéphane Bayen, Elvagris Segovia Estrada, Hui Zhang, Wei Kit Lee, Guillaume Juhel, Foppe Smedes, and Barry C. Kelly Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b06122 • Publication Date (Web): 28 Jan 2019 Downloaded from http://pubs.acs.org on January 30, 2019
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Partitioning and bioaccumulation of legacy and emerging hydrophobic organic chemicals
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in mangrove ecosystems.
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Stéphane Bayen*,1,2, Elvagris Segovia Estrada3, Hui Zhang4, Wei Kit Lee4, Guillaume Juhel5, Foppe
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Smedes6,7, Barry C. Kelly4
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of Food Science and Agricultural Chemistry, McGill University, 21111 Lakeshore, SteAnne-de-Bellevue, H9X 3V9, Quebec, Canada 2 Singapore-Delft Water Alliance, National University of Singapore, Block E1A #07-03, 1 Engineering Drive 2, Singapore 117576 3 Department of Geography, National University of Singapore, 1 Arts Link, AS2 #03-01, Singapore 117570 4 Department of Civil and Environmental Engineering, National University of Singapore, Block E1A #0703, 1 Engineering Drive 2, Singapore 117576 5 Tropical Marine Science Institute, National University of Singapore, 18 Kent Ridge Road Singapore 119227 6 Deltares, P.O. Box 85467, 3508 AL Utrecht, The Netherlands 7 Research Centre for Toxic Compounds in the Environment (RECETOX), Masaryk University, Kamenice 753/5, 625 00 Brno, Czech Republic
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*Corresponding author current address and email: Department of Food Science and Agricultural Chemistry McGill University, 21111 Lakeshore, Ste Anne de Bellevue Quebec, Canada, H9X 3V9
[email protected] 1 Department
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Abstract
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Knowledge regarding partitioning behavior and bioaccumulation potential of environmental
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contaminants is important for ecological and human health risk assessment. While a range of
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models are available to describe bioaccumulation potential of hydrophobic organic chemicals
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(HOCs) in temperate aquatic food webs, their applicability to tropical systems still needs to be
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validated. The present study involved field investigations to assess the occurrence, partitioning
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and bioaccumulation behavior of several legacy and emerging HOCs in mangrove ecosystems in
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Singapore. Concentrations of synthetic musk fragrance compounds, methyl triclosan (MTCS),
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polychlorinated biphenyls, organochlorine pesticides, and polycyclic aromatic hydrocarbons were
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measured in mangrove sediments, clams, and caged mussels. Freely dissolved concentrations of
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the HOCs in water were determined using silicone rubber passive samplers. Results showed that
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polycyclic musks and MTCS are present in mangrove ecosystems and can accumulate in the
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tissues of mollusks. The generated HOC concentration data for mangrove water, sediments and
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biota samples was further utilized to evaluate water-sediment partitioning (e.g. Koc values) and
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bioaccumulation behavior (e.g. BAF and BSAF values). Overall, the empirical models fit
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reasonably well with the data obtained for this ecosystem, supporting the concept that general
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models are applicable to predict the behavior of legacy and emerging HOCs in mangrove
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ecosystems.
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Keywords
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bioaccumulation factor; bioconcentration factor; contaminant of emerging concern;
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Introduction
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The global decline of estuarine and coastal ecosystems, including mangroves, is affecting a number
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of critical benefits, or ecosystem services 1, 2. Mangroves are considered to enhance fisheries and
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coastal protection and maintain among the highest densities of carbon of any ecosystem globally
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1.
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exposed to pollution from nearby upstream industrial areas or nearby oil palm plantations and
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aquaculture 3, discharge of domestic sewages 4 or marine pollutions such as oil spills 5. Although
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anthropogenic pollution is considered a threat to mangroves
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chemical contaminants is often limited in this habitat. Bayen
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polycyclic aromatic hydrocarbons (PAHs) and “conventional” persistent organic pollutants
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(POPs), there were virtually no data for other types of contaminants in mangrove ecosystems
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worldwide. Notably, there were little information on the so-called contaminants of emerging
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concern, such as industrial and commercial compounds, current-use pesticides, pharmaceuticals
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and personal care products. Personal care products include hydrophobic synthetic musk fragrance
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compounds, e.g. galaxolide (HHCB) which is used in consumer products such as shampoo,
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perfumed body cream, or hair conditioner
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toothpaste. These compounds enter the coastal environment via treated effluents from wastewater
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treatment plants.
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discrete sediment and organism samples at one near-shore mangrove site 11.
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Partition coefficients such as the organic carbon-water partition coefficient (Koc) and
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bioaccumulation metrics such as the bioaccumulation factor (BAF) are critical in the assessment
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of human health and ecological risk of contaminants. A range of models have been developed to
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describe these processes for hydrophobic organic chemicals (HOCs)
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developed for aquatic food webs in temperate climates, but their applicability to tropical or arctic
Because of their unique position in the intertidal region, mangrove tidal wetland habitats can be
9, 10.
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3, 6, 7, 7
the actual characterization of
noted that besides trace metals,
or the antibacterial agent triclosan (TCS) used in
Recently, synthetic musks and methyl triclosan (MTCS) were detected in
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Models have been
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food webs should be assessed cautiously
In fact, little is known about the bioaccumulative
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behavior and fate of HOCs in tropical regions 14. In 2004, the presence of legacy POPs and trace
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metals (e.g. Pb, Cd, Cu) was assessed at two mangrove sites in Singapore 15, 16. Results agreed with
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expected biomagnification of POPs, as their levels in tissues tended to increase with the trophic
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level. However, specificities have been recorded in other tropical systems, and Alava and Gobas
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14
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compared to arctic food webs. Recently, Zhang and Kelly 17 described the accumulation of HOCs
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in fish in tropical marine waters. In their study, freely dissolved concentrations computed using
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predictive models from the measured grab sample could provide a good correlation for
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bioaccumulation of coastal fish in Singapore 17. To the best of our knowledge, there is no other
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validation of bioaccumulation models for tropical systems and notably for intertidal mangrove
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ecosystems. A traditional approach to describe the partitioning of HOCs consists in collecting grab
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water or sediment samples 18. The direct measurement of HOCs in grab sample water can be quite
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challenging because the levels are generally very low. In addition, water quality in mangrove
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ecosystems can fluctuate tremendously over different time scales 7, and discrete grab water
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samples may not provide the representative information needed to characterize organisms'
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exposure for risk assessment. Alternatively, passive sampling techniques allow for time-integrated
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and biologically relevant measurements of trace chemicals in water. For example, silicon rubber
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(SR) passive samplers have the capacity to accumulate HOCs from water over days 19, and were
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used to measure their freely dissolved concentrations and interpret bioaccumulation for aquatic
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systems. To date, passive samplers have not been applied to investigate the behavior of a range of
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HOCs, and notably synthetic musks or TCS, in tropical marine waters.
observed differences in the biomagnification behavior of some HOCs in Galapagos sea lions as
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The overall objective was to provide a comprehensive assessment of the partitioning and
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bioaccumulation behavior of HOCs in tropical mangrove tidal wetland habitats. Specifically, the
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present study aimed to (i) assess the presence of a range of legacy and emerging HOCs in tropical
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mangrove ecosystems in Singapore, (ii) investigate partitioning and bioaccumulation behavior of
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HOCs in mangrove ecosystems using simultaneously passive samplers, caged (green mussels) and
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native organisms (lokan clams) to provide a highly accurate assessment of bioaccumulation
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potential based on freely dissolved concentrations and (iii) provide information regarding the
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bioaccumulation behavior of several emerging HOCs (synthetic musks and TCS), with direct
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comparison to well-studied, bioaccumulative substances (PCBs, OCPs, PAHs). Among the various
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environmental and biomonitoring approaches utilized for chemical risk assessment, bivalves (such
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as mussels and clams) have emerged globally as key sentinel species of aquatic systems (also
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called bioindicators) for both inorganic and organic contaminants
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larger study which also included the assessment of trace metals
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contaminants (e.g. pharmaceuticals, TCS, and bisphenol A)
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biomarkers, which will be presented in follow-up publications.
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20, 21.
This work was part of a
20,
relatively polar organic
and an integrated array of
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Material and methods
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Chemicals and Materials
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Analytical standards of the pesticides (mixture including aldrin (ALD), hexachlorobenzene
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(HCB), endosulfan sulfate (EDS) p,p’-DDT, p,p’-DDD, and p,p’-DDE), polychlorinated biphenyls
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(PCBs; mixture including congeners 8, 18, 28, 44, 52, 66, 77, 81, 101, 105, 114, 118, 123, 126,
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128, 138, 153, 156, 157, 167, 169, 170, 180, 187, 189, 195, 206, and 209), and PAHs (mixture
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including phenanthrene, fluoranthene, pyrene, benzo[b]fluoranthene, benzo[k]fluoranthene,
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benzo[a]pyrene) were obtained from AccuStandard (New Haven, CT, USA) and Sigma Aldrich
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(St. Louis, MO, USA). MTCS and synthetic musk fragrance compounds including celestolide
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(ADBI), phantolide (AHDI), traseolide (ATII), galaxolide (HHCB), tonalide (AHTN), musk
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xylene, musk moskene (MM), musk ambrette, and musk tibetene were obtained as individual
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standards from Dr. Ehrenstorfer GmbH (Augsburg, Germany). Isotopically labeled analogs (Table
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S1, see Supporting Information) were obtained from Dr. Ehrenstorfer GmbH, Cambridge Isotope
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Laboratories (Andover, MA, US) and Sigma Aldrich. Primary stock solutions (mixture of all
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individual analytes) were prepared in hexane and were stored at -20°C in the dark. Pesticide grade
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solvents were obtained from Fisher Scientific (Loughborough, UK) and Tedia (Fairfield, OH, US).
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Bio-Beads S-X3, 200-400 mesh size, were obtained from Bio-Rad (Hercules, CA, US). Anhydrous
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sodium sulfate and potassium hydroxide were purchased from Sigma Aldrich. Florisil (100-200
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mesh, Fisher Scientific) for cleanup was deactivated overnight at 300°C and reactivated with
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0.15% w/w of MilliQ water (Millipore). Glassware and metal equipment were baked at 300°C
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overnight, and rinsed consecutively with dichloromethane and hexane before use. Certified
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materials mussel SRM2974a and sediment SRM1944 were obtained from NIST (Gaithersburg,
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MD, US) for method validation.
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Passive samplers
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Silicon rubber sheets of 0.5 mm thickness were obtained from Altecweb.com. The material was
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cut in pieces (5.5×9.5 cm) that were pre-extracted by Soxhlet with ethylacetate for >100 h (about
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200 cycles). Subsequently the sheets were spiked with performance reference compounds (PRC)
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as described in Smedes and Booij
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occurring in technical mixtures, i.e. PCB 1, 2, 3, 10, 14, 21, 30, 50, 55, 78, 104, 145, and 204.
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Briefly, samplers were immersed in methanol in a ratio samplers (kg) to methanol (L) of 0.6 to 1
23.
PRC used were biphenyl-D10 and PCB congeners not
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and after adding the PRC spike solution (6-50 ng per sampler sheet depending on the PRC), placed
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on an orbital shaker (130 rpm and 2.5 cm amplitude). Then the methanol fraction was lowered step
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wise (~ 8%) in a two weeks period by adding water until 50%. This caused the PRC to be equally
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distributed over the sampler. The methanolic solution was then discarded, and after washing briefly
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with two liters of water, the samplers were packed in amber glass jars with stainless steel lined
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lids. From the release of PRCs spiked prior to deployment, the sampler-water exchange rate can
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be quantified 19 applying an appropriate model 24 using earlier published partition coefficients 25.
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Passive samplers were sandwiched into large aluminum wire mesh used as a holder to be attached
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on the cages.
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Field deployment and collection
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The field study was conducted at nine mangrove sites in Singapore as earlier described
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short, two identical rounds of deployment/sampling were conducted in October-November 2012
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and in June-July 2013 (later referred as the “2012” and “2013” samplings respectively).
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Meteorological conditions differed for both phases, with heavy rainfalls in the “2012”, and dry
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weather (haze event) in the “2013” sampling period. Meteorological conditions can influence
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pollutants’ loads or fate in mangrove ecosystems
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mussels (Perna viridis; 90±3 individuals per cage) were deployed in the water column for 28 or
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29 days. The small difference of 1 day between the two samplings was imposed by tides and
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calendar (access to the sites at low tide). Passive samplers were deployed in 2013 attached to the
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mussel cages (Figure S2) for the same period of time (n=2 per site). Green mussels live in the
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water column and have been successfully used as a bioindicators for legacy HOCs such as PCBs,
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1,1'-(2,2,2-Trichloroethane-1,1-diyl)bis(4-chlorobenzene) (p,p’-DDT) and PAHs 21, 27. At day 14,
7, 26.
20, 22.
In
For each site, three cages of Asian green
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three batches of lokan clams (Polymesoda expansa) and sediments were collected at each site.
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Lokan clams are widespread in the Southeast Asian mangroves and live buried or half-buried in
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sediments. Only a few studies have explored the use of lokan clams for pollution monitoring 15.
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Clams were found only at six of the nine mangrove sites (SITEs 1, 2, 4, 7, 8, and 9). For each cage
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of mussels and batch of clams, homogenized tissue samples were prepared by pooling together the
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soft tissues of 12-20 organisms depending on availability. Three composite sediment samples were
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collected (grab or manual sampling) from each site for both sampling years. Sediment
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homogenates were stored in glass jars at -20°C. Additional details on the field collection are
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presented in the supporting information (Method S1, Table S2). Water quality (temperature,
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conductivity, salinity, total dissolved solids, turbidity, pH, chlorophyll a, and dissolved oxygen),
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sediment organic content and biometric data for the organisms (shell length, biomass, and
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condition index) were reported earlier 20, 22. Tissue and sediment dry weights were determined as
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the remaining fraction after drying 48 h at 60°C (Methods S2 and S3).
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Silicon rubber passive sampler extraction
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Upon collection, passive samplers were gently cleaned for fouling, transported on ice to the
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laboratory individually wrapped in solvent-rinsed aluminum foil and stored at -20°C until
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extraction. Extraction and analysis have been described in a comprehensive technical document
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by Smedes and Booij 23. In short, samples were cold extracted with twice 150 mL of methanol.
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Extracts were combined and their volume was reduced using rotary evaporators. Extract cleanup
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was conducted on a Florisil mini-column (Pasteur pipette) containing 1 g of deactivated Florisil
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and 1 g of sodium sulfate and eluted with 40 mL of hexane: dichloromethane 1:1 (v/v). Extracts
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were then concentrated under a gentle flow of nitrogen. Chemical analyses were conducted using
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gas chromatography-electron impact tandem mass spectrometry (GC-EI-MS/MS) for all the
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compounds of interest. Two unexposed passive samplers were used to measure the initial quantity
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of PRCs spiked in the passive samplers. Freely dissolved concentrations (Cw), measured in the
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water column where the mussel cages were deployed, were calculated using published models 19,
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24, 25
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information, Method S4).
for semi-volatile compounds (Details on this procedure are provided in the supporting
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Extraction of HOCs from bivalve tissues
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HOCs were extracted from bivalve soft tissues using microwave assisted extraction following the
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standard operating protocol ME017 by Milestone 28. In short, 1.0±0.1 g of fresh tissues (or 0.2 g
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in the case of freeze-dried certified material) was transferred to the extraction vessel and mass–
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labeled surrogates (i.e. deuterated or
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equilibration for about 30 minutes. Four mL of methanolic potassium hydroxide (1M) were added
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and then 10 mL of hexane and extracted in an Ethos system (Milestone, Italy). After cooling down,
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the extract was transferred to a clean conical flask, after going through a 1 g sodium sulfate mini-
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column (Pasteur Pipette fitted with a glass wool plug). After concentration to 1 mL in a rotary
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evaporator, extracts went through gel permeation chromatography (Bio-Beads S-X3) using 250
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mL of hexane-dichloromethane 1:1 v/v (the first 90 mL was discarded and the next 160 mL
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collected). After concentration in a rotary evaporator, the extract was further cleaned on a Florisil
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mini-column as described above for passive samplers. Extracts were finally concentrated under a
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gentle flow of nitrogen to
