Marine Pollution Bulletin 93 (2015) 266–269

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Persistent organic pollutants and polycyclic aromatic hydrocarbons in mosses after fire at the Brazilian Antarctic Station Fernanda Imperatrice Colabuono a,⇑, Satie Taniguchi a, Caio Vinícius Zecchin Cipro a,b, Josilene da Silva a, Márcia Caruso Bícego a, Rosalinda Carmela Montone a a b

Laboratório de Química Orgânica Marinha, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brazil Littoral Environnement et Sociétés (LIENSs), UMR 7266, CNRS-Université de La Rochelle, 2 rue Olympe de Gouges, 17042 La Rochelle Cedex 01, France

a r t i c l e

i n f o

Article history: Available online 7 February 2015 Keywords: Antarctic vegetation PCBs HCB PBDEs PAHs Fire emissions

a b s t r a c t A fire at the Brazilian Antarctic Station on February 25th, 2012 led to the burning of material that produced organic pollutants. To evaluate the impact in the surrounding area, polycyclic aromatic hydrocarbons (PAHs) and persistent organic pollutants (POPs) were analyzed in moss samples collected in the vicinities of the station before and after the incident and compared to findings from previous studies in the same region. PCBs were on the same magnitude as that reported in previous studies, which could be associated to the global dispersion of these compounds and may not be related to the local fire. In contrast, concentrations of HCB and PAHs were higher than those reported in previous studies. No PBDEs were found above the method detection limit. Organic contaminant concentrations in mosses decreased a few months after the fire, which is an important characteristic when considering the use of mosses for monitoring recent exposure. Ó 2015 Elsevier Ltd. All rights reserved.

Located on King George Island (South Shetland Archipelago) in Admiralty Bay (62°100 S; 58°240 W), the Brazilian Antarctic Station was established in 1984 as a research station and is occupied throughout the year by both scientific and military personnel. On February 25th, 2012, a large fire occurred at the station, destroying 70% of the facilities (Guerra et al., 2013), including the research laboratories, materials, equipment, personal belongings and the energy generators (four powered by Arctic diesel and one by ethanol). The combustion process can send semi-volatile organic pollutants into the environment. Polycyclic aromatic hydrocarbons (PAHs) and persistent organic pollutants (POPs) are common contaminants produced by a wide variety of combustion sources, such as plastics, wood, fuel and other chemicals (Lohmann et al., 2000; Breivik et al., 2004; Barber et al., 2005). These pollutants are released into the atmosphere, dispersed and deposited in the environment (Meharg et al., 1998). Vegetation and soil are generally the first receptors of atmospheric pollutants (Simonich and Hites 1994, 1995). Mosses constitute one of the principal components of terrestrial flora in the Antarctic ecosystem, whose nutrient supply depends largely on atmospheric deposition (Borghini et al., 2005). Since ⇑ Corresponding author. E-mail address: fi[email protected] (F.I. Colabuono). http://dx.doi.org/10.1016/j.marpolbul.2015.01.018 0025-326X/Ó 2015 Elsevier Ltd. All rights reserved.

mosses have no root system or cuticle, they absorb/adsorb nutrients and contaminants directly from the environment; they are also relatively easy to collect (Harmens et al., 2011). Thus, mosses can play a very important role as biomonitors and long-term integrators of persistent contaminant depositions and have been used extensively in environmental pollution studies throughout the world (Yogui and Sericano, 2008; Cipro et al., 2011; Ciesielczuk et al., 2012). PAHs, hexachlorobenzene (HCB), polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) were analyzed in moss samples collected in the vicinities of Brazilian Antarctic Station before and after the incident to evaluate the impact in the surrounding area. The concentrations of other chlorinated compounds were also evaluated, such as DDT and HCHs, which, although not closely related with fire, are important pollutants in polar regions. The data were compared with findings described in previous contamination studies in the same region. Moss samples were collected from areas adjacent to the Brazilian Antarctic Station (Fig. 1), in Admiralty Bay, on King George Island during the austral summer. Two sampling campaigns were performed: the first was in March 2012, less than one month after the fire, and the second was in December 2012, about eight months after the fire. In March 2012, seven samples of Sanionia uncinata were collected from six different sites (Sites 1–6) and one sample of Warnstorfia sarmentosa was collected from Site 1. In December

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2012, two samples of S. uncinata were collected (Sites 3 and 7). Due to the removal of debris and modifications to the environment around the Brazilian Antarctic Station, sampling could not be performed at exactly the same sites during the second campaign. Samples of Brachitecyum sp. (n = 1), Syntrichia princeps (n = 2) and S. uncinata (n = 7) collected in December 2004/January 2005 (Sites 5, 7–9, 11–12) in a previous campaign were analyzed for the determination of the concentrations of organic contaminants prior to the fire. All vegetation was collected manually, stored in aluminum containers and kept frozen at 20 °C until analysis. The analytical procedure followed that described by MacLeod et al. (1985) with minor modifications. Briefly, 3 g of dry sample was extracted in a Soxhlet apparatus for 8 h using 80 ml of n-hexane and methylene chloride (1:1, v/v). Before extraction, the surrogates d8-naphthalene, d10-acenaphthene, d10-phenanthrene, d12-chrysene and d12-perylene (for PAHs), 2,20 ,4,50 ,6-pentachlorobiphenyl and 2,20 ,3,30 ,4,5,50 ,6-octachlorobiphenyl (for PCBs, OCPs and PBDEs) were added to all samples, blanks and reference material. The extracts were cleaned using column chromatography with 8 g of silica and 16 g of alumina (both 5% water deactivated) and eluted with 80 ml of n-hexane and methylene chloride (1:1, v/ v). The internal standards 2,4,5,6-tetrachlorometaxylene (TCMX) and d10-fluorene and d12-benzo[b]fluoranthene were added before the gas chromatographic analysis. A procedural blank was included in each analytical batch. Identification and quantification of organochlorine pesticides were performed with a gas chromatograph (6890 N Agilent Technologies) coupled to an electron capture detector (GC-ECD) using a 30 m  0.25 mm i.d. capillary column coated with 5% phenylsubstituted dimethylpolysiloxane phase (film thickness: 0.5 lm). Automatic splitless injections of 2 ll were applied and the total purge rate was adjusted to 50 ml min1. Hydrogen was used as the carrier gas (constant pressure of 40 kPa at 100 °C), while nitrogen was the make up gas at a rate of 60 ml min1. Parental PAHs and their alkyl substituted compounds, PCBs and PBDEs were quantitatively analyzed using a gas chromatograph (5973 N Agilent Technologies) coupled to a mass spectrometer (GC/MS) in selected ion mode (SIM 70 eV), using the same column employed for GC-ECD. The volume injected was 1 lL in automatic splitless

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mode. Helium was used as the carrier gas (constant flow of 1.1 ml min1). For quality assurance/quality control (QA/QC), the analytical method was validated using a standard reference (SRM 1945) purchased from the National Institute of Standards and Technology (NIST, USA). SRM 1945 was analyzed in duplicate and the average recovery of analytes was within the range accepted by the NS&T (Wade and Cantillo, 1994). The recovery of analytes in spiked blanks and matrices produced satisfactory results (67–115%). Analytes in laboratory blanks were subtracted from the samples. The quantification of analytes was performed using a nine-level analytical curve and followed the internal standard procedure. Method quantification limits (QL) ranged (in ng g1 dry weight) from < 0.19 to 0.47 for OCPs, < 0.30 to 1.09 for PCBs, < 0.76 to 1.06 for PBDEs and < 1.14 to 10.3 for PAHs. When summing compound classes, concentrations below the QL were set to zero. Table 1 shows the mean concentrations of organic pollutants from mosses sampled from areas surrounding the Brazilian Antarctic Station, in Admiralty Bay, and data from previous studies in the same region. Individual concentrations are presented as supplementary data. PCBs are usually the dominant contaminant in moss samples from Antarctica (Bacci et al., 1986; Borghini et al., 2005; Cipro et al., 2011; Wu et al., 2014). Mosses sampled after the fire (March/2012) showed a different pattern: low concentrations of PCBs and a predominance of HCB (see discussion below). Tri-, tetra- and penta-CBs were prevalent in moss samples and hexa-CBs were also detected (supplementary data: Table S1). HCB concentrations increased of one order of magnitude soon after the fire at the Brazilian Antarctic Station, but the levels were restored about eight months later and were similar to those reported by Cipro et al. (2011) from previous years (Table 1; supplementary data: Table S2). Studies from other locations in Antarctica also report that HCB concentrations are generally low in mosses. For example, Bacci et al. (1986) and Cabrerizo et al. (2012) found HCB concentrations of 0.49 ng g1 (dw) and 0.02 to 0.12 ng g1 (dw), respectively, in mosses from the Antarctic Peninsula, while Borghini et al. (2005) found HCB levels from 0.82 to 1.95 ng g1 (dw) on Victoria Land in the Ross Sea. Although HCB

Fig. 1. Sampling site on King George Island in Admiralty Bay, Antarctica (Site 1: Brazilian Antarctic Station).

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Table 1 P Concentrations (mean ± SD) of organic contaminants (ng g1 dry weight) found in moss samples from Admiralty Bay, Antarctica. PCBs = total sum of polychlorinated biphenyls, P P P PBDEs = total sum of polybrominated diphenyl ethers, DDTs = sum of p,p’-DDT, o,p’-DDT, p,p’-DDE, o,p’-DDE, p,p’- DDD and o,p’- DDD, HCH = sum of a-, b-, d- and G-isomer, P P Drins = sum of aldrin, endrin, isodrin and dieldrin, PAHs = total sum of polycyclic aromatic hydrocarbons. P P P P P P Species Date PCBs PBDEs DDTs HCHs Drins HCB PAHs Reference Sanionia uncinata (n = 6) Sanionia uncinata (n = 6) Brachitecyum sp. (n = 1)

1992–1993 1993–1994 2004–2005

7.97 ± 7.87 – 1.57 ± 0.54 – 0.28a 15.7a

– – 1.22a

– – n.d.a

– – –

– – 0.78a

Syntrichia princeps (n = 2)

2004–2005

16.8a

1.73a

n.d.a

–

1.06a

Sanionia uncinata (n = 7)

2004–2005

18.6 ± 2.5a 0.89 ± 0.28a 1.62 ± 0.58a 1.20 ± 0.81a –

0.81 ± 0.18a

Sanionia uncinata (n = 11) Sanionia uncinata (n = 7) Warnstorfia sarmentosa (n = 1) Sanionia uncinata (n = 2)

2005–2006 March – 2012 March – 2012 December – 2012

– 1.64 ± 1.73 n.d. 1.59–1.96

– 15.8 ± 12.1 19.8 n.d. – 2.76

0.72a

0.82 ± 0.27 n.d. n.d n.d.

– 1.93 ± 2.85 n.d. n.d.

is a relatively volatile compound used in agriculture and industry that can be transported to cold regions due to the global distillation effect, it can be also released into the environment by incomplete combustion (Barber et al., 2005). Thus, the higher concentrations found only in mosses collected in March of 2012 may be related to emissions resulting from the fire at the Brazilian station. Organochlorine contaminants not derived from the fire, such as DDTs (mainly p,p0 -DDE) and HCHs (c-HCH), also occurred in mosses sampled in 2012 (Table 1; supplementary data: Table S2), but at levels on the same order of magnitude as that reported in previous studies conducted in the same region (Cipro et al., 2011) as well as in other areas of Antarctica (Borghini et al., 2005). These organochlorine pollutants have been found in Antarctic organisms for decades (Bacci et al., 1986; Corsolini, 2009), and the presence of these compounds in moss samples could be associated with global dispersion. Chlordanes, methoxychlor, endosulfan and mirex concentrations were below the method detection limit in the moss samples. PBDEs were also not detected in the present study, although these compounds have been previously reported at low levels in mosses from Admiralty Bay (Yogui and Sericano, 2008; Cipro et al., 2011). The concentrations of total PAHs ranged from 131 to 1235 ng g1 (dw) in March 2012 and from 126 to 254 ng g1 (dw) in December 2012 (supplementary data: Table S3). No PAHs were detected in moss samples before the fire (Table 1). Mosses usually reflect the concentrations and distribution of PAHs in the

– 2.91 ± 0.48 n.d. 1.48–1.57

– 1.59 ± 2.19 n.d. n.d.

– – n.d.b

Montone (1995) Montone (1995) Cipro et al. (2011)a/ this workb n.d.b Cipro et al. (2011)a/ this workb n.d.b Cipro et al. (2011)a/ this workb – Yogui and Sericano (2008) 544 ± 457 This work 955 This work 126–254 This work

atmosphere (Thomas, 1984) and are able to absorb PAHs from the air and precipitation, subsequently releasing these compounds mainly by wash-off, evaporation and/or degradation (Wu et al., 2014). The increase in PAH concentrations just after the fire and the slight decrease observed about eight months later are the result of the input of PAHs stemming from the fire. Compounds with two to four rings accounted for 81% and 95% of the total PAHs in moss samples in March 2012 and December 2012, respectively. Moreover, a predominance of naphthalene and its alkyl substituted homologues was found, mainly in samples collected one month after the fire (Fig. 2). Arctic grade diesel fuel is the main energy source in Antarctic operations and contains mainly semi-volatile aromatic hydrocarbons, such as naphthalene and other non-substituted PAHs with two or three aromatic rings, with a relatively high concentration of corresponding alkyl-substituted hydrocarbons (Kennicutt et al., 1991). PAHs with five or six aromatic rings with minimal alkylated products are frequently related to combustion processes (Colombo et al., 1989; Yunker et al., 2002). The retene, identified in most of the moss samples collected after the fire, is a pyrolysis-derived compound and it is usually associated to wood combustion (Ramdahl, 1983). After emission into the atmosphere, the most volatile PAHs remain in a gaseous phase, whereas less volatile PAHs (5 or 6 rings) are adsorbed to solid atmospheric particles (Harmes et al. 2011). Vegetation can remove 26–62% of atmospheric PAHs through the uptake of compounds in both the gaseous and particulate phases

Fig. 2. Mean and standard deviation of concentrations of individual polycyclic aromatic hydrocarbons in moss samples from Admiralty Bay, Antarctica, after the fire at Brazilian Antarctic Station; Acronyms: NA – naphthalene, ANA – sum of alkylnaphthalenes, BP -biphenyl, AC – acenaphthene, FL - fluorene, AFL – sum of alkylfluorenes, DBT – dibenzothiophene, ADBT – sum of alkyldibenzothiophenes, PHE – phenanthrene, AN – anthracene, APHE – alkylphenanthrenes, FA – fluoranthene, AFA – alkylfluoranthenes, PY – Pyrene, APY – sum of alkylpyrene, RET – retene, B[a]AN – benzo[a]anthracene, CHR – chrysene, ACHR – sum of alkylchrysenes, B[b]FA – benzo[a]fluoranthene, B[k]FA – benzo[k]fluoranthene, B[j]FA – benzo[j]fluoranthene, B[e]PY – benz[e]pyrene, B[a]PY – benzo[a]pyrene, B[b]CHR – benzo[b]chrysene, PR – perylene, IPY – indeno [1,2,3-cd]pyrene, DB[ah]AN – dibenzo[ah]anthracene, B[ghi]PR – benzo[ghi]perylene.

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(Thomas, 1986; Simonich and Hites, 1994). The presence of the low molecular PAHs and their alkyl-substituted homologues can be attributed to the volatilization of the Arctic grade diesel fuel due to the fire. On the other hand, the heavy five-ring and six-ring PAHs can be formed due to pyrolysis during the fire. Therefore, the PAHs detected were related to the fire in the Brazilian Antarctic Station and their concentrations gradually decreased over time. Mosses proved to be a useful matrix for the assessment of POPs and PAHs in the atmosphere around the Brazilian Antarctic Station, where the fire took place. The findings indicate the introduction of contaminants, such as HCB and PAHs, due to the incident. PCBs may not be related to the fire and are more likely to be from remote sources. In general, the concentrations of organic contaminants in mosses decreased a few months after the fire, which is an important characteristic to consider when using mosses for monitoring recent exposure. Acknowledgments Financial support was provided by the Brazilian Ministry of the Environment (MMA) as part of the ‘‘Environmental monitoring in the direct influence area of the Brazilian Antarctic Station’’. The National Science and Technology Institute on Antarctic Environmental Research (INCT-APA) and the Brazilian Antarctic Program (PROANTAR) provided logistic support in Antarctica. The authors are also grateful to Dr. Jair Putzke (Universidade de Santa Cruz do Sul) and Dr. Antonio Pereira Batista (Universidade Federal do Pampa) for assistance in the identification of moss species. F.I. Colabuono received a research grant from the Fundação de Amparo a Pesquisa do Estado de São Paulo (Fapesp). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.marpolbul.2015. 01.018. References Bacci, E., Calamari, D., Gaggi, C., Fanelli, R., Focardi, S., Morosini, M., 1986. Chlorinated hydrocarbons in lichen and moss samples from Antarctic Peninsula. Chemosphere 15, 747–754. Barber, J.L., Sweetman, A.J., Wijk, D., Jones, K.C., 2005. Hexachlorobenzene in the global environment: emissions, levels, distribution, trends and processes. Sci. Total Environ. 349, 1–44. Borghini, F., Grimalt, J.O., Sanchez-Hernandez, J.C., Bargagli, R., 2005. Organochlorine pollutants in soils and mosses from Victoria Land (Antarctica). Chemosphere 58, 271–278. Breivik, K., Alcock, R., Li, Y., Bailey, R.B., Fiedler, H., Pacyna, J.M., 2004. Primary sources of selected POPs: regional and global scale emission inventories. Environ. Pollut. 128, 3–16.

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