Polybrominated diphenyl ether flame retardants in lichens and mosses

from King George Island, maritime Antarctica

G.T. Yogui *, J.L. Sericano

Geochemical and Environmental Research Group, College of Geosciences, Texas A&M University, 833 Graham Road, College Station, TX 77845, USA

article info

Article history:

Received 5 July 2008

Received in revised form 25 August 2008

Accepted 26 August 2008

Available online 11 October 2008

Keywords:

PBDEs

Persistent organic pollutants

Sanionia uncinata

Usnea antarctica

Usnea aurantiaco-atra

Antarctic Peninsula

abstract

Lichens and mosses are considered good indicators of atmospheric pollution as they absorb contaminants

directly from the air. Polybrominated diphenyl ethers (PBDEs) are man-made chemicals used as flame

retardants in materials such as plastics, textiles, electronic circuitry and furnishing foam. Few studies

have investigated PBDEs in the southern hemisphere including Antarctica. This paper presents the first

evaluation of PBDEs in lichens (Usnea antarctica and Usnea aurantiaco-atra) and mosses (Sanionia uncinata) collected at King George Island, maritime Antarctica. PBDEs were detected at low levels in all lichen

and moss samples. On average, the levels of PBDEs in mosses (818 pg g1 dry weight; 101 ng g1 lipid)

were significantly higher than in lichens (168 pg g1 dry weight; 9.11 ng g1 lipid). This difference is most

likely due to the differing mechanisms of PBDEs uptake from the atmosphere which are controlled by a

number of chemical, environmental and plant variables. Contaminant concentrations were not statistically different at sites close to and distant from human facilities. Long-range atmospheric transport is

believed to be the primary source of PBDEs to King George Island. The pattern of congeners in plants

resembles those found in commercial mixtures of Penta-BDE. In addition, the presence of BDE-183 in

lichens and mosses suggests that other technical formulations (e.g., Octa-BDE and Deca-BDE) have

reached Antarctica. Further studies are needed to better understand the role of Antarctic vegetation as

a sink for anthropogenic organic pollutants.

2008 Elsevier Ltd. All rights reserved.

1. Introduction

Polybrominated diphenyl ethers (PBDEs) have been used as

flame retardants to prevent the risk of fire in polymeric materials

(e.g., plastics, textiles and furnishing foam). Historically, the world

production of these chemicals has been limited to few companies

located in the northern hemisphere (de Wit, 2002 and references

therein). However, there is evidence of their widespread distribution throughout the global environment (e.g., de Boer et al., 1998;

Corsolini et al., 2006; de Wit et al., 2006). Some authors have argued

that PBDEs qualify as persistent organic pollutants (POPs) due to

their long-range transport, persistency in the environment, bioaccumulation and toxicity to organisms (e.g., de Wit et al., 2006).

Vegetation has been used to monitor organic pollution since the

early 1980s (see Buckley, 1982). The major uptake mechanism of

lipophilic organic contaminants by vegetation is partitioning from

air to plant tissue at the leaf surface. This pathway is a function of

the physical–chemical properties of the contaminant (e.g., lipophilicity and vapor pressure), environmental conditions (e.g., temperature) and plant species (Simonich and Hites, 1995).

Furthermore, Morosini et al. (1993) have found a correlation between levels of organic contaminants in vegetation and the surrounding air, suggesting that vegetation integrates atmospheric

contamination over time.

The distribution of terrestrial vegetation in Antarctica is limited

to ice-free areas which are primarily found along the mainland

coast and adjacent islands. Plant species have been recorded

throughout Antarctica from its northernmost limit (60 S, according to the Antarctic Treaty) poleward to the Trans Antarctic Mountains at latitude of 86 S (Peat et al., 2007). Plant communities are

dominated by lower plants (predominantly lichens and mosses)

and biodiversity tends to decline with increasing latitude. Peat

et al. (2007) divided the Antarctic flora into three major provinces

namely northern maritime, southern maritime and continental.

Species richness is highest in the northern maritime Antarctica

and is characterized by approximately 350 lichens, 115 mosses,

27 liverworts and 2 phanerogams (Peat et al., 2007).

The lichens Usnea antarctica Du Rietz and Usnea aurantiaco-atra

(Jacq.) Bory along with the moss Sanionia uncinata (Hedw.) Loeske

are commonly found in the Antarctic tundra (Osyczka et al., 2007).

U. antarctica has a circumpolar distribution with greatest abundances along the Antarctic Peninsula. U. aurantiaco-atra is less

ubiquitous than its counterpart and is restricted to the South Orkney Islands, South Shetland Islands and the Antarctic Peninsula.

The moss S. uncinata is a bipolar species and has widespread

0045-6535/$ - see front matter 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.chemosphere.2008.08.035

* Corresponding author. Tel.: +1 979 862 2323x167; fax: +1 979 862 2361.

E-mail address: gtyogui@ocean.tamu.edu (G.T. Yogui).

Chemosphere 73 (2008) 1589–1593

Contents lists available at ScienceDirect

Chemosphere

journal homepage: www.elsevier.com/locate/chemosphere
distribution along the western Antarctic Peninsula (Smith, 1996;

Øvstedal and Lewis-Smith, 2001; Shaw, 2001). These three species

have been used as bioindicators of atmospheric pollution in Antarctica because of their dominant occurrence in ice-free areas and

ease of sampling (e.g., Mietelski et al., 2000; Osyczka et al., 2007).

Monitoring studies using lichens and mosses in the western

Antarctic Peninsula have investigated trace metals, radioactive elements and chlorinated hydrocarbons (Bacci et al., 1986; Poblet

et al., 1997; Godoy et al., 1998; Olech et al., 1998; Mietelski

et al., 2000; Schuller et al., 2002; Osyczka et al., 2007). There appears to be no data published on PBDEs in Antarctic vegetation.

This study presents the first evaluation of PBDEs in the lichens

and mosses of King George Island, Antarctica.

2. Material and methods

2.1. Sampling and study area

King George is the largest island in the South Shetlands archipelago and is located approximately 120 km north of the Antarctic

Peninsula (Fig. 1). Over 90% of its 1300 km2 is ice-covered (RakusaSuszczewski, 1980). Admiralty Bay is the largest fjord-like embayment on King George Island encompassing a surface area of

122 km2 (Rakusa-Suszczewski et al., 1993). The coast of Admiralty

Bay is fairly irregular alternating between gravel/sandy beaches,

rocky shores and glaciers along its ca. 84 km long shoreline (Rakusa-Suszczewski, 1995). Lichens and mosses were collected at 11

sampling sites during the austral summer 2005–2006 in ice-free,

coastal areas of Admiralty Bay (Fig. 1). Samples were collected by

hand (with latex gloves) and thoroughly shaken to remove extraneous material such as animal-related debris and soil particles.

All samples were stored in clean glass jars and frozen at 20 C

as soon as possible.

2.2. Chemical analysis

All plant samples were homogenized in the laboratory prior to

analysis. Extraction and clean-up followed standard procedures

routinely used at the Geochemical and Environmental Research

Group (GERG) and published elsewhere (e.g., Lauenstein and Cantillo, 1998). Briefly, approximately 10 g of wet plant tissue was

mixed with 40 g of anhydrous sodium sulfate and extracted with

300 mL of dichloromethane using a tissumizer (PRO Scientific

Inc., model PRO250). Plant extracts were extensively cleaned up

with sulfuric acid, silica/alumina chromatography and gel permeation chromatography/high performance liquid chromatography

(GPC/HPLC). Dry and lipid weights were gravimetrically determined using an analytical balance following standard procedures

used at the GERG facilities.

2.3. Instrumental parameters

Sample extracts were injected into a GC–MS (Agilent Technologies) in the selected ion monitoring (SIM) mode. A HP-5 ms capillary column (30 m length  0.25 mm id  0.25 lm film thickness)

was used for separation of compounds. Helium was used as carrier

gas under constant flow (0.8 mL min1

) into the column. The oven

temperature was programmed as follows: 130 C for 1 min,

ramped at 12 C min1 to 154 C, ramped at 2 C min1 to 210 C

and ramped at 3 C min1 to 300 C with a final hold time of

5 min. The mass spectrometer was operated in EI mode. The ion

stacking technique was employed to increase the GC–MS sensitivity so that ultra-trace analyte concentrations could be detected

(Yogui, 2008). This technique consists of recording the intensity

of a particular ion several times during a single scan cycle of the

MS detector. The SIM run was divided into seven functions where

each m/z ion was recorded 6–12 times per scan cycle.

2.4. Quality control

Quality control criteria were based on Lauenstein and Cantillo

(1998) and EPA (2003). Quantitation of the target analytes used

isotope dilution and internal standard techniques. The following

13C-labeled standards were used: BDEs 15, 28, 47, 77, 99, 100,

118, 126, 153 and 183. The average recovery of internal standards

was 66 ± 2.8% (95% level of confidence). In each analytical batch,

East

Antarctica

West

Antarctica

60o W 58o W 56o W

63.5o S

62.5o S

61.5o S

King George South Shetland Islands

Island

Bransfield Strait

Antarctic Peninsula

58.6o W 58.5o W 58.4o W 58.3o W 58.2o W

62.2oS

62.1oS

Ferraz Station

(Brazil)

King George

Island

Field Station

(Ecuador) Machu Picchu Station

(Peru)

Arctowski Station

(Poland) Pieter J.Lenie

Field Station

(USA)

Admiralty

Bay

Bransfield Strait

5 km

Fig. 1. Location of the study area and sampling sites. Refer to Table 1 for sampling site codes.

1590 G.T. Yogui, J.L. Sericano / Chemosphere 73 (2008) 1589–1593
two matrices were spiked with PBDEs and analyzed in duplicate.

The mean recovery of PBDE standards in the spiked matrices was

106 ± 3.9% (95% level of confidence). The relative percent difference (RPD) between the spiked duplicates was 17 ± 3% (95% level

of confidence). The limits of detection for selected major PBDEs

found in samples were 1.0 pg g1 dry weight (BDEs 15, 47 and

49), 1.4 pg g1 dry weight (BDEs 99 and 100) and 1.3 pg g1 dry

weight (BDEs 153 and 154).

2.5. Statistical analyses

Single-factor ANOVA and two-factor ANOVA (Model I, fixed effects) were performed to compare population means. The ANOVA

is a robust, parametric test used to infer statistically significant differences between two or more population means. Assumptions of

the test are: (1) data are independent and continuous; (2) data

are approximately normally distributed; and (3) data set variances

are homogeneous (Dytham, 2003). Distribution of PBDEs in plant

tissues was skewed. So the data sets were transformed using natural logarithm to meet the assumptions of the ANOVA. This is a

valid alternative as long as all data points are systematically converted using the same procedure (Ott and Longnecker, 2001).

Simonich and Hites (1995) recommended that concentration of organic pollutants in vegetation be normalized to lipid basis when

comparing different species. This approach accounts for some of

the variability due to biochemical differences in plants. In this

study, all statistical evaluations were performed on lipid-normalized data. The critical level of significance of the statistical analyses

was set at a = 0.05.

3. Results and discussion

A suite of 36 di- through hepta-BDEs was measured including

the following congeners: 7, 8, 10, 11, 12, 13, 15, 17, 25, 28, 30,

32, 33, 35, 37, 47, 49, 66, 71, 75, 77, 85, 99, 100, 116, 118, 119,

126, 138, 153, 154, 155, 166, 181, 183 and 190 (numeration

according to the same IUPAC system used for PCBs). However, only

BDEs 15, 28, 33, 47, 49, 66, 85, 99, 100, 153, 154 and 183 were detected above the method detection limits. It is important to note

that hexa-BDEs (IUPAC Nos. 138, 153, 154, 155 and 166) could

not be identified and quantified in the moss S. uncinata because

of interfering peaks that remained in the extracts after extensive

purification.

The average total PBDEs in lichens of the species U. antarctica

was 192 pg g1 dry weight (n = 6, SD = 93.9) while in the species

U. aurantiaco-atra was 139 pg g1 dry weight (n = 5, SD = 33.6)

(Table 1). According to the single-factor ANOVA, there is no significant difference between PBDEs in the two lichen species (F = 0.77,

df = 1, p > 0.05). Poblet et al. (1997) also did not find a statistical

difference in the accumulation of metals (Fe, Zn, Pb and Cd) by

U. antarctica and U. aurantiaco-atra collected at King George Island.

Genetic and morphological investigations have revealed a very

close relationship between these two species, supporting the

hypotheses that they might be a single species, or alternatively

constitute a species pair where U. antarctica would be the sterile

form and U. aurantiaco-atra the fertile form (Walker, 1985; Seymour et al., 2007). Based on these reports and the statistical results, both lichen species are pooled as a single species for

purposes of comparison with mosses of the species S. uncinata.

Concentrations of PBDEs in lichens and mosses collected along

the shore of Admiralty Bay are shown in Tables 1 and 2. A two-factor model I (fixed effects) ANOVA was performed to determine the

effects of plant species and human presence on concentration of

PBDEs. Each of the main factors (i.e., plant species and human presence) had two levels. Plant species was grouped as lichens and

mosses, whereas human presence was grouped as sampling sites

close to (sites A–F) and distant from (sites G–K) the Brazilian scientific station (see Fig. 1). The ANOVA indicated that PBDE levels

Table 1

Concentration of PBDEs (pg g1 dry weight) in lichens collected along the shore of Admiralty Bay, King George Island, Antarctica

Site Location Species Dry weight (%) Lipid (%) BDE-47

(pg g1 dry weight)

BDE-99

(pg g1 dry weight)

BDE-100

(pg g1 dry weight)

PPBDEs

(pg g1 dry weight)

A Refuge 2 U. aurantiaco-atra 87.0 1.18 37.4 42.2 8.12 98.3

B Plaza Point U. antarctica 85.5 2.87 65.5 74.9 14.9 179

C Ferraz (chemistry) U. aurantiaco-atra 86.5 1.20 70.0 63.7 12.7 182

D Ferraz (VLF) U. aurantiaco-atra 85.2 1.10 49.9 41.4 8.58 116

E Stenhouse Point U. antarctica 89.4 2.01 48.7 42.9 8.20 114

F Ullman Point U. aurantiaco-atra 87.3 1.15 57.9 67.2 13.2 160

G Hennequin Point U. antarctica 82.2 2.02 64.0 72.6 14.8 176

H Vauréal Cape U. antarctica 87.7 1.94 138 155 32.5 377

I Demay Point U. antarctica 87.1 1.80 55.3 55.6 11.4 157

J Ezcurra Inlet U. aurantiaco-atra 86.9 1.61 54.1 58.6 11.4 140

K Machu Picchu U. antarctica 88.1 1.44 51.8 59.4 11.4 148

Average ± standard deviation 86.6 ± 1.9 1.67 ± 0.54 63.0 ± 26.5 66.7 ± 31.7 13.4 ± 6.8 168 ± 75

Table 2

Concentration of PBDEs (pg g1 dry weight) in mosses collected along the shore of Admiralty Bay, King George Island, Antarctica

Site Location Species Dry weight (%) Lipid (%) BDE-47

(pg g1 dry weight)

BDE-99

(pg g1 dry weight)

BDE-100

(pg g1 dry weight)

PPBDEs

(pg g1 dry weight)

A Refuge 2 S. uncinata 55.9 0.278 403 402 80.2 960

B Plaza Point S. uncinata 49.0 0.493 377 564 106 1137

C Ferraz (chemistry) S. uncinata 18.2 0.128 303 457 100 883

D Ferraz (VLF) S. uncinata 33.9 0.114 132 130 36.5 319

E Stenhouse Point S. uncinata 72.8 1.41 206 312 82.5 630

F Ullman Point S. uncinata 41.4 0.328 180 250 71.4 538

G Hennequin Point S. uncinata 55.7 0.379 193 283 69.9 584

H Vauréal Cape S. uncinata 12.4 0.124 404 579 123 1184

I Demay Point S. uncinata 71.5 1.37 375 513 81.8 1020

J Ezcurra Inlet S. uncinata 13.2 0.105 315 383 93.2 834

K Machu Picchu S. uncinata 70.3 0.799 343 431 81.8 912

Average ± standard deviation 44.9 ± 23.0 0.50 ± 0.49 294 ± 99 391 ± 139 84.2 ± 22.3 818 ± 270

G.T. Yogui, J.L. Sericano / Chemosphere 73 (2008) 1589–1593 1591
were not influenced by main factors interaction (F = 0.12, df = 1,

p > 0.05). The mean total PBDEs in mosses was significantly higher

than in lichens (F = 144, df = 1, p < 0.0001). However, there was no

significant difference in contamination levels close to (sites A–F)

and distant from (sites G–K) the Brazilian scientific station

(F = 0.07, df = 1, p > 0.05).

Along the shore of Admiralty Bay, there are three scientific stations (Arctowski, Poland; Ferraz, Brazil; and Machu Picchu, Peru)

and two field stations (USA and Ecuador). Arctowski and Ferraz

are occupied year round while the others have activities limited

to summer (and are often unoccupied even in the summer in the

case of Peru and Ecuador). Considering that Ferraz is the largest

station in Admiralty Bay, it is reasonable to assume that it will

cause the greatest human impact in the area. The statistical analysis revealed no contamination difference in sampling sites close to

and distant from Ferraz station, suggesting that station activities

are not a significant source of PBDEs to the local environment. Indeed, no significant local input of POPs (e.g., PCBs) has been detected in the area and long-range atmospheric transport is

believed to be the primary source of these chemicals to Admiralty

Bay (Montone et al., 2003; Montone et al., 2005). In contrast, a recent study found high PBDE levels in indoor dust and wastewater

sludge from McMurdo (USA) and Scott (New Zealand) research

bases, showing that human activities may be a local source of

PBDEs to the Antarctic environment (Hale et al., 2008). McMurdo

and Scott bases – located within 3 km from each other – host over

1000 people during the summer. This far exceeds human occupation at the Brazilian station which hosts approximately 50 people

each summer. Taking into account the recent findings of Hale

et al. (2008), local sources of PBDEs to Admiralty Bay cannot be totally ruled out. Human facilities such as the Brazilian and the Polish

stations may be a complimentary source of brominated flame

retardants to the local environment. It is suggested that PBDEs

be analyzed in indoor dust and wastewater sludge of local research

stations in order to investigate their potential as local sources of

contaminants.

The average percent distribution of PBDEs in lichens and mosses

was similar (Fig. 2). Tetra-BDEs represented 38% of the total PBDEs

in both lichens and mosses, whereas penta-BDEs averaged 47% in

lichens and 58% in mosses. This is similar to commercial formulations of Penta-BDE which are 24–38% tetra-BDEs, 50–60% pentaBDEs and 4–8% hexa-BDEs (de Wit, 2002). Congener pattern

similarities between Antarctic vegetation and the Penta-BDE mixture suggest that PBDEs do not undergo major fractionation during

their long-range transport to Antarctica although minor fractionation may occur. IUPAC Nos. 47, 99 and 100 were the three major

congeners detected in all samples, accounting for more than 75% of

total PBDEs. This agrees with other studies worldwide (see de Wit,

2002).

Di- and tri-BDEs occur at trace amounts in Penta-BDE formulations (La Guardia et al., 2006). Minor proportions of BDE-15 and

BDE-28/33 (co-eluted) in the Antarctic samples may be explained

by either global fractionation or degradation of more highly brominated congeners. Global fractionation preferentially transports

more volatile chemicals to sites farther away from their emission

areas as compared to less volatile organic compounds (Wania

and Mackay, 1993). It has also been reported that PBDEs undergo

photochemical debromination (e.g., Eriksson et al., 2004; Keum

and Li, 2005; Ahn et al., 2006; Rayne et al., 2006). Thus, it is reasonable to assume that transformation processes may alter PBDE mixtures during long-range atmospheric transport to Antarctica. In

addition, degradation might also take place at the plant surface

as suggested by Simonich and Hites (1995). Detection of the heptabrominated BDE-183 in lichens and mosses implies that technical

mixtures other than the Penta-BDE formulation have reached the

Antarctic environment. BDE-183 is a major congener present in

the Octa-BDE product (La Guardia et al., 2006). According to Bezares-Cruz et al. (2004), BDE-183 may also be a degradation product

of BDE-209 which is the dominant congener in the Deca-BDE formulation – the most widely produced PBDE commercial mixture.

Differences in contamination of lichens and mosses are most

likely associated with processes responsible for PBDEs uptake from

the atmosphere which are complex and may be governed by a

number of chemical, environmental and plant parameters. HexaBDEs (i.e., BDEs 153 and 154) represented approximately 8% of

the total PBDEs in lichens. Taking into consideration that these

congeners could not be measured in mosses and are usually detected in environmental samples, it is reasonable to suggest that

PBDEs concentrations in mosses are somewhat higher than the

reported values. This confirms the differences observed in the

ANOVA that higher levels of PBDEs occur in mosses when compared to lichens.

Other pollution monitoring studies in the western Antarctic

Peninsula have observed differential contaminant accumulation

in lichens and mosses. Osyczka et al. (2007) found greater concentration of trace elements in the moss S. uncinata when compared to

lichens U. antarctica and U. aurantiaco-atra. Mietelski et al. (2000)

observed fractionation of radionuclides between mosses and lichens. While S. uncinata is non-selective with regard to 137Cs and 241Am from atmospheric fallout, these radioactive elements seem

to be leached out of U. antarctica and U. aurantiaco-atra. Godoy

et al. (1998) also observed greater accumulation of 137Cs in several

moss species in comparison with lichens from the South Shetland

Islands.

There are few data published on PBDEs in lichens and mosses. A

comprehensive study in northern Russia collected plants (including lichens and mosses) from several sites (AMAP, 2004). However,

BDEs 47 and 99 were not found above the limit of detection

(0.2 ng g1 dry weight) in any sample (AMAP, 2004). Moss samples

from two locations in Norway revealed total PBDE concentrations

of 149 pg g1 wet weight and 328 pg g1 wet weight (de Wit

et al., 2006 and a reference therein). These levels are similar to

those reported here. On a wet basis, the mean total PBDEs in

mosses collected at King George Island was 363 pg g1 wet weight

(range: 108–729 pg g1 wet weight). In the 1980s, Bacci et al.

(1986) investigated chlorinated hydrocarbons in mosses and lichens of the western Antarctic Peninsula. Levels of HCB, a-HCH,

c-HCH, p,p0-DDT and p,p0-DDE at that time are comparable to levels

of PBDEs reported in this study (carried out 20 years later). However, the concentration of PCBs measured in the 1980s is an order

0

20

40

60

80

di- tri- tetra- penta- hexa- heptaBDE Homolog Series

Percentage (%)

Penta-BDE

Lichen

Moss

Fig. 2. Percent distribution of PBDE homologs in the commercial penta-BDE

formulation compared to lichens and mosses collected along the shore of Admiralty

Bay, King George Island, Antarctica.

1592 G.T. Yogui, J.L. Sericano / Chemosphere 73 (2008) 1589–1593
of magnitude higher than the PBDE contamination in this study

(Bacci et al., 1986).

PBDEs were detected in all lichen and moss samples. These species absorb PBDEs directly from the atmosphere as they lack rootlike structures. Long-range atmospheric transport is believed to be

the major source of PBDEs to King George Island since contamination is not statistically different at sites close to and distant from

human facilities. Mosses evidenced contamination levels significantly higher than lichens. This is likely associated with the primary process responsible for PBDEs uptake from the atmosphere

which may be governed by a number of chemical, environmental

and plant properties. Further studies are needed to better understand the role of Antarctic vegetation as a sink for anthropogenic

organic pollutants.

Acknowledgements

The authors are thankful to Dr. Rosalinda Montone for the

opportunity to participate in the Antarctic expeditions, and Dr.

Chuck Kennicutt, Dr. Terry Wade and Dr. Miguel Mora for comments on this manuscript. Mr. Filipe Victoria and Mr. Adriano

Spielmann deserve credit for the identification of plant species.

Field trips to collect samples in Antarctica were financially supported by the Brazilian Antarctic Program (CNPq Project Number

55.0348/02-6; Environmental Management of Admiralty Bay, King

George Island, Antarctica: POPs and sewage pollution) and the College of Geosciences at Texas A&M University (through the Pipes

Endowed Fellowship). G. T. Yogui was funded by Coordenação de

Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Ministry

of Education, Brazil.

Appendix A. Supplementary material

Supplementary data associated with this article can be found, in

the online version, at doi:10.1016/j.chemosphere.2008.08.035.

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