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Trophic Magnification of Parabens and Their Metabolites in a Subtropical Marine Food Web Xiaohong Xue, Jingchuan Xue, Wenbin Liu, Douglas H. Adams, and Kurunthachalam Kannan Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.6b05501 • Publication Date (Web): 13 Dec 2016 Downloaded from http://pubs.acs.org on December 22, 2016
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Trophic Magnification of Parabens and Their Metabolites in a
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Subtropical Marine Food Web
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Xiaohong Xue1,2, Jingchuan Xue1, Wenbin Liu1,3, Douglas H. Adams4, Kurunthachalam Kannan1,5* 1
Wadsworth Center, New York State Department of Health, and Department of Environmental Health Sciences, School of Public Health, State University of New York at Albany, Empire State Plaza, P.O. Box 509, Albany, NY 12201-0509, USA
2
Environmental Engineering Institute, Department of Physics, Dalian Maritime University, 1 Linghai Road, Dalian 116026, Liaoning, China
3
State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 100085 Beijing, China
4
Florida Fish & Wildlife Conservation Commission, Fish & Wildlife Research Institute, 1220 Prospect Avenue #285, Melbourne, FL 32901, USA
5
Biochemistry Department, Faculty of Science and Experimental Biochemistry Unit, King Fahd Medical Research Center, King Abdulaziz University, Jeddah, Saudi Arabia
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*Corresponding author: K. Kannan Wadsworth Center Empire State Plaza, P.O. Box 509 Albany, NY 12201-0509 Tel: +1-518-474-0015 Fax: +1-518-473-2895 E-mail:
[email protected] For submission to: ES&T
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TOC:
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known about bioaccumulation of these chemicals in aquatic environments. In this study, six
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parabens and four of their common metabolites were measured in abiotic (water, sediment) and
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biotic (fish, invertebrates, plants) samples collected from a subtropical marine food web in
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coastal Florida. Methyl paraben (MeP) was found in all abiotic (100%) and a majority of biotic
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(87%) samples. 4-Hydroxy benzoic acid (4-HB) was the most abundant metabolite, found in 99%
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of biotic and all abiotic samples analyzed. The food chain accumulation of MeP and 4-HB was
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investigated for this food web. The trophic magnification factor (TMF) of MeP was estimated to
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be 1.83, which suggests considerable biomagnification of this compound in the marine food web.
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In contrast, a low TMF value was found for 4-HB (0.30), indicating that this compound is
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metabolized and excreted along the food web. This is the first study to document the widespread
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occurrence of parabens and their metabolites in fish, invertebrates, seagrasses, marine
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macroalgae, mangroves, sea water, and ocean sediments and to elucidate biomagnification
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potential of MeP in a marine food web.
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Key words: parabens; benzoic acid; 4-HB; TMF; marine food web; trophic transfer;
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biomagnification
Abstract: Despite the widespread use of parabens in a range of consumer products, little is
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Introduction
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Parabens are alkyl esters of p-hydroxybenzoic acid that are used as preservatives in foodstuffs,
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personal care products, and pharmaceuticals, due to their stability, water solubility, and
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broad-spectrum antimicrobial activity.1 The most commonly used parabens include
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methyl-paraben (MeP), ethyl-paraben (EtP), propyl-paraben (PrP), butyl-paraben (BuP),
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heptyl-paraben (HeP), and benzyl-paraben (BzP). 4-Hydroxybenzoic acid (4-HB) and
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3,4-dihydroxybenzoic acid (3,4-DHB) are the common metabolites of parabens.2,3 In addition,
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methyl-protocatechuate (OH-MeP) and ethyl-protocatechuate (OH-EtP) are hydroxylation
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products of MeP and EtP, respectively, a common mechanism for biotic and abiotic
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transformation of many xenobiotics.4 Although parabens are considered generally safe, in vivo
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and in vitro studies have shown the endocrine-disrupting effects of these chemicals.1,5-12
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Parabens and their metabolites have been found in various environmental media, including
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indoor dust, wastewater, and sewage sludge, among others.13-18 These substances also have been
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found in a variety of human specimens, including urine, serum, placenta, and breast tumor
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tissues.19-23 4-HB concentrations of up to 17400 ng/g were reported in human adipose tissue.24
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Recently, we reported an elevated accumulation of parabens and their metabolites in marine
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mammals, fish, and birds.25,26 These studies provide insight into the bioaccumulation potential of
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parabens. Nevertheless, studies that describe the accumulation of parabens in organisms at
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various trophic levels in the food web are not available. Therefore, in this study, we collected
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abiotic (water and sediment) and biotic (seagrasses, mangroves, marine macroalgae,
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invertebrates, and fish) samples from a marine food web in Florida coastal waters in the United
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States to investigate the trophic transfer and biomagnification of parabens and their metabolites.
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This is the first report on the occurrence and distribution of these chemicals in a variety of fish
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and invertebrate species, seagrasses, marine macroalgae, mangroves, sea water, and sediment
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from coastal estuarine and marine environments.
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Materials and Methods
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Sample Collection. All abiotic and biotic samples analyzed in this study were collected
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from Florida coastal waters, primarily along the Indian River Lagoon and adjacent offshore
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waters, by the Florida Fish and Wildlife Research Institute’s Fisheries-Independent Monitoring
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Program during 2015–2016. Sampling for the estuarine component of this study occurred within
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the Indian River Lagoon from Ponce de Leon Inlet (29° 04’ N) south to the Vero Beach area (27°
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39’ N) within all three major basins of the system (Mosquito Lagoon, Indian River Lagoon
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proper, and Banana River Lagoon). Sampling for the offshore component occurred in adjacent
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Atlantic Ocean waters from Ponce de Leon Inlet (29° 04’ N) south to Jupiter Inlet (26° 56’ N). A
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map that shows estuarine sampling locations and adjacent Atlantic Ocean areas is presented in
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Figure S1. A total of 167 tissue samples (liver, kidney, and homogenized skin-on whole fish)
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from 35 species of fish were collected and include shortfin mako (Isurus oxyrinchus), spinner
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shark
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(Carcharhinus limbatus), great hammerhead shark (Sphyrna mokarran), bonnethead shark
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(Sphyrna tiburo), Atlantic stingray (Dasyatis sabina), bonefish (Albula vulpes), bay anchovy
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(Anchoa mitchilli), scaled sardine (Harengula jaguana), Atlantic thread herring (Opisthonema
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oglinum), inshore lizardfish (Synodus foetens), striped mullet (Mugil cephalus), rough silverside
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(Membras martinica), Atlantic silverside (Menidia menidia), leopard searobin (Prionotus
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scitulus), common snook (Centropomus undecimalis), black sea bass (Centropristis striata), gag
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(Mycteroperca microlepis), bluefish (Pomatomus saltatrix), Florida pompano (Trachinotus
(Carcharhinus
brevipinna),
bull
shark
(Carcharhinus
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blacktip
shark
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carolinus), red snapper (Lutjanus campechanus), gray snapper (Lutjanus griseus), pigfish
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(Orthopristis chrysoperta), sea bream (Archosargus rhomboidalis), sheepshead (Archosargus
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probatocephalus), pinfish (Lagodon rhomboides), silver perch (Bairdiella chrysoura), spotted
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seatrout (Cynoscion nebulosus), Atlantic croaker (Micropogonias undulatus), red drum
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(Sciaenops ocellatus), Spanish mackerel (Scomberomorus maculatus), bay whiff (Citharichthys
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spilopterus), southern flounder (Paralichthys lethostigma), and gray triggerfish (Balistes
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capriscus). A total of 39 invertebrates, representing 18 species, were collected, including sponge
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(Halichondria melanodocia), tunicate (Styela plicata), bigclaw snapping shrimp (Alpheus
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heterochaelis),
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(Farfantepenaeusaztecus), Florida grass shrimp (Palaemon floridanus), penaeid shrimp
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(Penaeidae), pink shrimp (Farfantepeneaus duoarum), ivory barnacle (Amphibalanus eburneus),
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blue crab (Callinectes sapidus), mud crab (Scylla spp.), thin stripe hermit crab (Clibanarius
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vittatus), cross-barred venus (Chione elevata), hard clam (Mercinaria mercinaria), eastern oyster
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(Crassostrea virginica), Florida crown conch (Melongena corona), pear whelk (Busyconspiratum
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pyruloides), and Atlantic brief squid (Lolliguncula brevis). Three seagrass species, manatee grass
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(Syringodium filiforme), shoal grass (Halodule wrightii), and widgeon grass (Ruppia martima),
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were analyzed. A species of green alga, Caulerpa prolifera, also was analyzed. Three mangrove
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species, black mangrove (Avicennia germinans), red mangrove (Rhizophora mangle), and white
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mangrove (Laguncularia racemosa), also were analyzed. In addition, six surface water and eight
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surface sediment samples were collected along the Florida coast, at representative estuarine and
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coastal ocean locations where biological samples had been collected.
Atlantic
white
shrimp
(Litopenaeus
setiferus),
brown
shrimp
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Liver and/or kidney tissues were collected from some fish species, whereas skin-on whole
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fish samples were analyzed from other species (Table S1). For each invertebrate, the whole body
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(soft tissue) was analyzed. Whole fish and invertebrates were homogenized using an
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Ultra-Turrax homogenizer (IKA, Staufen, Germany). For invertebrate species with exoskeletons
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or hard shells (e.g., shrimp, crab, snails), the exoskeletons or shells were removed before
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homogenization. For mangrove species, leaves, stems, and propagules were homogenized and
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analyzed. For seagrass samples, both rhizomes and blades were homogenized. All samples were
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stored at -20° C until further analysis. Detailed information with regard to samples, including
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date of collection, body length, and body weight, are shown in Table S1.
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Sample Preparation.
The sample preparation procedure for the analysis of parabens and
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their metabolites in biologic samples (liver, kidney, skin-on whole fish/invertebrate samples,
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seagrass, green alga, and mangrove samples) has been described elsewhere.27-29 For liver and
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kidney tissues, the surface of each tissue sample was removed with clean scissors and tweezers
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to prevent potential extraneous contamination during necropsy and storage. Then, 200 to 300 mg
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of tissue and 1000 mg of seagrass, green alga, and mangrove were accurately weighed and
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spiked with 50 ng of IS mixture (13C6-MeP, 13C6-BuP, d4-HeP, d4-BzP, and 13C6-4-HB). Five mL
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of acetone were added to the sample after equilibration for 30 min. The mixture was
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homogenized in a mortar and transferred to a 15 mL polypropylene (PP) tube by washing with a
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2 mL mixture of methanol and acetonitrile (1:1, v/v). The combined extracts were shaken in an
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oscillator shaker for 60 min and then centrifuged at 5000 × g for 5 min (Eppendorf Centrifuge
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5804, Hamburg, Germany). The supernatant was then concentrated to near dryness under a
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gentle nitrogen stream. One mL of a mixture of methanol and acetonitrile (1:1, v/v) was added,
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and after storage at -20° C overnight and immediate centrifugation at 5000 × g for 5 min, the
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supernatant was transferred into a vial for liquid chromatography tandem mass spectrometric
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(HPLC-MS/MS) analysis.
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Analytical protocols for parabens and their metabolites in sea water and sediment samples
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were similar with those described earlier, with minor modifications.30 Briefly, 500 mL of sea
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water were filtered through a cellulose nitrate membrane filter (47 mm, pore size 0.45 µm; GE
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Healthcare UK Limited, Buckinghamshire, UK) to separate suspended particulate matter (SPM).
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A known volume of acidified Milli-Q water (formic acid, 0.2%; pH = 2.5) was added to each
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water sample to adjust to pH 5. Then a mixture of IS (100 ng) was spiked prior to extraction. An
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Oasis® MCX 6 cm3 (150 mg; Waters, Milford, MA) solid-phase extraction (SPE) cartridge was
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used to extract the target analytes from the water samples. Prior to the loading of samples, the
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cartridge was pre-conditioned with 10 mL of methanol and 10 mL of Milli-Q water with 0.2%
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formic acid. Then the cartridge was washed with acidified Milli-Q water (formic acid, 0.2%)
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before drying for ∼30 min under a vacuum. Nine mL of methanol were used to elute the target
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chemicals. The eluents were concentrated to one mL under a gentle stream of nitrogen, using a
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TurboVap evaporator (Zymark Inc., Hopkinton, MA).
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For the analysis of sediments, ∼0.4 g of freeze-dried sediment was spiked with a mixture of
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IS (50 ng) prior to extraction. Then sediment samples were extracted with 5 mL of
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methanol/water mixture (5:3; v/v) by shaking in an orbital shaker for 60 min and sonicating for
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30 min. Extracts were centrifuged at 5000 x g for 5 min (Eppendorf Centrifuge 5804, Hamburg,
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Germany), the supernatant was collected in a PP tube, and the extraction was repeated twice. The
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supernatants were combined and concentrated to ∼3 mL under a gentle nitrogen stream and then
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diluted to 10 mL with Milli-Q water that contained 0.2% formic acid. The extract was purified
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with the SPE procedure, as described above.
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Instrumental Analysis.
An Agilent 1100 Series HPLC system (Agilent Technologies Inc.,
Santa Clara, CA) connected to an Applied Biosystems API 2000 electrospray triple quadrupole
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mass spectrometer (ESI-MS/MS; Applied Biosystems, Foster City, CA) was used in the analysis.
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A Zorbax® SB-Aq (150 mm × 2.1 mm, 3.5 µm) column, serially connected to a Javelin guard
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column (Betasil® C18, 20 mm × 2.1 mm, 5 µm), was used for the separation of target analytes.
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The injection volume was 10 µL, and the mobile phase comprised methanol (A) and Milli-Q
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water that contained 0.4% (v/v) acetic acid (B). The target compounds were separated by
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gradient elution at a flow rate of 300 µL/min, starting at 5% (v/v) A, held for 3 min, increased to
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85% A within 2 min, held for 1 min, further increased to 98% A within 2 min, held for 7 min, and
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reverted to 5% A at the 16th min and held for 7 min. The MS/MS was operated in the negative
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ion multiple reaction monitoring mode. Nitrogen was used as the curtain and collision gas at
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flow rates of 20 and 2 psi, respectively. The electrospray ionization voltage was set at -4.5 kV.
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The source heater was set at 450° C. The nebulizer gas (ion source gas 1) was set at 55 psi, and
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the heater gas (ion source gas 2) was set at 70 psi. The data acquisition was performed at a scan
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speed of 25 ms and a resolving power of 0.70 full width at half-maximum.
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Quality Assurance and Quality Control (QA/QC).
The QA/QC procedures have been
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described in the supplementary information. Method limits of quantification (MLOQs) for liver,
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kidney, and muscle were similar to those reported in our previous study.26 MLOQs for
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homogenized skin-on whole fish samples and invertebrate samples were similar to those reported
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for muscle in our earlier study. MLOQs for plants samples were 2.32 ng/g for six parent parabens,
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5.81 ng/g for OH-MeP and OH-EtP, and 58.1 ng/g for 3,4-DHB and 4-HB. MLOQs for parabens
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in sea water and sediments were similar to those reported for wastewater and sludge samples in
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our earlier study.30
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Stable Isotope Analysis and Trophic Level Determination.
For the determination of the
food web structure and trophic position of each of the organisms analyzed, stable nitrogen (δ15N)
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and stable carbon (δ13C) isotope analyses were performed on fish liver, kidney, whole fish,
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invertebrate soft tissue, mangrove, and seagrass samples at the Environmental Isotope
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Laboratory, University of Waterloo, Ontario, Canada.31 The analysis was performed by
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combustion of sample material to gas through an 1108 Elemental Analyzer (Fisons, Ipswich,
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UK), coupled to a Delta Plus (Thermo, Waltham, MA) continuous flow isotope ratio mass
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spectrometer (CFIRMS). Trophic levels (TLs) of individual organisms were determined based on
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the assumption that zooplankton occupies TL 2.0, based on the following equation (1):32
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TLconsumer = 2 + (δ15Nconsumer - δ15Nbaseline )/3.8
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In this study, the average values of Florida crown conch and hard clam were used to estimate the
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δ15N baseline.33 The δ15N baseline equals 9.09, and 3.8 is the enrichment factor constant.34,35
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Trophic Magnification Factor (TMF).
(1)
TMFs were calculated according to a method
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reported previously.33 The calculation is based on the relationship between TL and parabens
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concentrations:
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Ln concentration [wet weight (ww)] = a + (b × TL)
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in which a is the y-intercept (constant). TMFs for each contaminant were then determined from
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the slope b of eq 2 using the following eq (3):
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TMF = eb
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A TMF value between 0 and 1 indicates that the contaminant is not biomagnified in the food web,
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whereas TMF > 1 indicates that the contaminant biomagnifies in the food web.32
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(2)
(3)
Data Analysis.
Details with regard to data analysis have been provided in the
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supplementary information. A robust regression-on-order statistics (ROS) was employed for the
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left-censored data in this study.36, 37
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Results and Discussion
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Parabens and their Metabolites in Coastal Water and Sediments. Six sea water and eight
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sediment samples from representative estuarine and coastal marine locations were analyzed
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(Table 1). MeP and EtP were present in all sea water samples analyzed at mean concentrations of
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14.7 ± 10.9 (range: 3.02–31.7) and 6.12 ±7 .09 (range: 0.52–17.2) ng/L, respectively (Tables 1
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and S2). PrP was found in three of six sea water samples at concentrations that ranged from < 0.5
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to 9.04 ng/L (Table S2). Other parabens were less frequently detected, with detection rates (DRs)
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that ranged from 16.7% to 33% (Table S2). 4-HB was the only metabolite found in all sea water
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samples, at an average concentration of 439 ± 191 ng/L (range: 219–753 ng/L; Table S2).
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MeP and EtP were found in all sediment samples at mean (±SD) concentrations of 3.03 ±
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2.79 (range: 0.85–9.00) and 7.06 ± 3.53 (range: 2.15–12.4) ng/g, dry wt, respectively (Tables 1
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and S2). No other parabens were found in sediments. Of the four paraben metabolites measured,
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4-HB was the most abundant compound found in all sediment samples (mean ± SD: 55.4 ± 42.2;
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range: 20.3–141 ng/g; Table 1). 3,4-DHB and OH-MeP were found in sediments at a DR of 50%
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and 38%, respectively (Table S2); nevertheless, the two metabolites were not present in sea
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water samples. This indicates biological transformation (e.g., transformation of parent parabens
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into their metabolites) of parabens in sediment. A significant positive correlation was found
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between ln[MeP] and ln[4-HB] (r = 0.74, p = 0.04, Figure 1a). This suggests a common source
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for MeP and 4-HB or transformation/interconversion of MeP and 4-HB by methylating and
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demethylating microorganisms in sediments.38
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Of note is that the highest concentrations of MeP and 4-HB in sediment (MeP: 9 ng/g; 4-HB:
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141 ng/g) and water (MeP: 31.7 ng/L; 4-HB: 753 ng/L) were found in those samples collected
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from Banana River Lagoon Basin. This may be related to the discharge of wastewater or other
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human activities at the military or aerospace facilities adjacent to the sample collection sites in
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this area.
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Parabens and their Metabolites in Marine Biota. Of the six parent parabens measured,
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MeP was the predominant compound found in 203 of 226 (90%) marine biota samples analyzed
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(Table 1). The highest MeP concentration was found in the kidney of a red snapper (610 ng/g
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wet wt; Table 1). EtP, PrP, BuP, and BzP were found at a DR of 1.33% to 7.52% (Table S2).
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Among paraben metabolites, 4-HB was the most abundant compound, found in 99% of the biota
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samples analyzed (Table 1). The highest 4-HB concentration was found in a cross-barred venus
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(68,100 ng/g, wet wt; Table 1), a marine bivalve mollusk that feeds primarily on phytoplankton
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and microprotozoa from the water column. The cross-barred venus is frequently preyed upon by
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multiple gastropod species as well as portunid crab species. The black drum (Pogonias cromis)
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and red drum (Sciaenops ocellatus) also prey on this clam species (personal observation, D.
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Adams). Human health-related issues have been reported due to the consumption of this clam
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species because brevetoxins bind strongly to the lipids of this clam at high concentrations.39 It is
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possible that MeP also binds to the lipids present in this species. The other three metabolites
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analyzed were found in several invertebrate species, including the cross-barred venus, sponge,
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thin stripe hermit crab, tunicate, and ivory barnacle, at a DR of 1.33% to 15% (Table S2).
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MeP was found in all (n = 9) seagrass samples (mean ± SD: 19.1 ± 13.4; range: 4.04–42.0
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ng/g) and all (n = 13) mangrove samples (mean ± SD: 18.5 ± 7.83; range: 8.00–33.3 ng/g) (Table
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1), and these concentrations were higher than those found in green alga. EtP, BuP, and BzP were
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also found in some (4.5%–13.6%) seagrass and mangrove samples (Table S2). 3,4-DHB and
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4-HB were found in all marine plant samples (Tables 1 and S2). Mean (±SD) concentrations of
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4-HB and 3,4-DHB in seagrass samples were 4640 (±4920) (range: 216–15700) and 782 (±959)
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(range: 91.9–2830) ng/g, respectively (Tables 1 and S2). Mangrove samples contained
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comparable 4-HB concentrations (mean ± SD: 2650 ± 948; range: 1020–4420 ng/g) and much
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higher levels of 3,4-DHB (mean ± SD: 3180 ± 4300; range: 189–13500 ng/g) (Tables 1 and S2).
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Green alga had the lowest concentrations of 4-HB (mean ± SD: 134 ± 106; range: 28.2–273 ng/g)
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and 3,4-DHB (mean ± SD: 238 ± 220; range: 64.1–523 ng/g). Within the mangrove species, the
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MeP concentration in black mangroves (mean ± SD: 30.2 ± 4.91; range: 24.5–33.3 ng/g) was
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approximately two times greater than that found in red mangroves (mean ± SD: 14.7 ± 2.38;
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range: 12.3–16.9) and white mangroves (mean ± SD: 15.2 ± 5.27; range: 8–21.1). However,
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4-HB concentrations in black mangroves (mean ± SD: 3430 ± 882; range: 2750–4420 ng/g) and
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red mangroves (mean ± SD: 3170 ± 708; range: 2160–3820) were generally similar but higher
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than the concentrations detected in white mangroves (mean ± SD: 1910 ± 555; range: 1020–
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2400). Black mangroves have been believed to exhibit greater capacity in metal accumulation
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than do other mangrove species due to the higher active root tissue in metal exclusion and
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sequestration processes.40 The same mechanism also may work for organic contaminants. No
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significant spatial variations in concentrations of MeP and 4-HB were found within each species.
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Seagrasses have been reported to produce some of these phenolic acids.41 OH-MeP was found in
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8 of 9 seagrass samples and 7 of 13 mangrove samples at concentrations that ranged from
