Changes and Variations of Polycyclic Aromatic Hydrocarbon

ARTICLE IN PRESS

Marine Pollution Bulletin xxx (2010) xxx–xxx

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Marine Pollution Bulletin

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Baseline Changes and variations of polycyclic aromatic hydrocarbon concentrations in ﬁsh, barnacles and crabs following an oil spill in a mangrove of Guanabara Bay, Southeast Brazil

Abílio Soares-Gomes a, Roberta L. Neves b, Ricardo Aucélio b, Paulo H. Van Der Ven c, Fábio B. Pitombo a, Carla L.T. Mendes a, Roberta L. Ziolli b,* a Laboratório de Ecologia de Sedimento, Departamento de Biologia Marinha, Universidade Federal Fluminense, Caixa Postal 100644, Niterói, RJ 24001-970, Brazil b Laboratório de Estudos Ambientais e Toxicologia (LEATox), Departamento de Química, Pontifícia Universidade Católica do Rio de Janeiro (PUC-Rio), Rua Marquês de São Vicente, 225, Gávea, Rio de Janeiro, RJ 22453-900, Brazil c Vale Moçambique Ltda, Vila Carbomoc Casa 20, Moatize, Tete, Mozambique article info abstract

Keywords: On April 26th, 2005, an accident caused a leak of 60,000 L of Diesel Oil Type ‘‘B”, freighted by train wagons Polycyclic aromatic hydrocarbons upstream on a mangrove area within Guanabara Bay, Southeast Brazil. After the accident, samples from Oil spill animals with different biological requirements were collected in order to monitor polycyclic aromatic Crabs hydrocarbons concentrations for the following 12 months. Sessile, mobile, carnivorous, omnivorous, Barnacles organic detritus feeders, planktivorous and suspension feeders were some of the attributes compared. Fish Concentrations of PAHs did not vary in relation to different dietary habits and the best response was from Sentinel À1 Guanabara Bay the sessile suspensivorous barnacles. A background level of <50 lgkg was suggested based on the reference site and on values observed in the following months after the accident. The highest values of PAH concentrations were observed in barnacles in the ﬁrst month immediately after the spill, decreasing to background levels after few months. Barnacles are suggested as a sentinel species. Ó 2010 Elsevier Ltd. All rights reserved.

On April 26th, 2005, an accident took place on the railway oper- mours and cancer (Hoffman, 2003). Relationships between the ated by ‘‘Ferrovia Centro-Atlântica” (FCA), in Itaboraí municipality, occurrence of neoplasia and liver tumours in fish and PAH concen- Rio de Janeiro State. The accident caused the leakage of 60,000 L of trations in sediment where they were collected have shown that diesel oil freighted by train wagons. Part of the oil was retained on- there is a strong causal link between these factors (Malins et al., site and part reached the Aldeia and Caceribú Rivers (Fig. 1). In 1988; Varanasi, 1989; Hoffman, 2003; Ariese et al., 2005). Polycy- spite of the immediate containment work, the oil was spread over clic aromatic hydrocarbons affect humans primarily through food by the river and through the mangrove channels of Caceribu estu- consumption. Once ingested, PAHs can be absorbed by the human ary, within the Guapimirim Environmental Protected Area [‘‘APA body and may cause cancers and decreased fecundity, among other de Guapimirim”], driven by tidal flow. The spill product was clas- health problems (Fleming et al., 2006). Besides ecological conse- sified as Diesel Oil Type ‘‘B”, used as fuel by automotive vehicles. quences, seafood safety is an issue of concern in every oil spill inci- After the accident, FCA contacted scientific institutions and consul- dent. Commercial and recreational fisheries and subsistence tants to begin monitoring the effects of the oil on biota, specially seafood use could potentially be affected as a consequence of the edible organisms. It is in this scope that this present research plays fauna and flora exposure to oil. In order to guarantee public health, its role, being part of the environmental studies developed volun- restrictions or closure of seafood harvesting might be necessary tarily by FCA and under the supervision of the Brazilian Federal (Yender et al., 2002). In Brazil, determining safety concentration Environmental Agency, Instituto Chico Mendes de Conservação levels of PAHs in seafood exposed to oil is usually dealt with in da Diversidade (ICMBIO). workshops developed on the occasion of the spill, with the partic- Polycyclic aromatic hydrocarbons (PAHs) affect organisms ipation of the State staff and federal agencies, and the responsible through toxic actions. A major concern in animals is the ability of party. To date, no agency has adopted clear guidelines for fisheries the reactive metabolites of some PAHs to bind cellular proteins closure or reopening after an incident of oil environmental con- and DNA, leading to mutations, developmental malformations, tu- tamination (Silva et al., 2007). Since the affected areas were within a mangrove environment, * Corresponding author. Tel.: +55 21 3527 1824; fax: +55 21 3527 1637. used by the local fisherman to catch crabs and finfish for selling E-mail address: [email protected] (R.L. Ziolli). at nearby markets, the main concern of this study was to assess

Please cite this article in press as: Soares-Gomes, A., et al. Changes and variations of polycyclic aromatic hydrocarbon concentrations in ﬁsh, barnacles and crabs following an oil spill in a mangrove of Guanabara Bay, Southeast Brazil. Mar. Pollut. Bull. (2010), doi:10.1016/j.marpolbul.2010.05.013 ARTICLE IN PRESS

2 A. Soares-Gomes et al. / Marine Pollution Bulletin xxx (2010) xxx–xxx

Mage Itaborai

Duque de Caxias

Sao Goncalo

Guanabara Bay

Rio de Janeiro Niteroi

5km Atlanctic Ocean

430 2'30''W 430 0'0''W 420 57'30''W 420 55'0''W N

railway

main road Caceribu River cafoecalPtnedic

S''03'2422 Aldeia River

Guanabara Bay

Mangrove

S''0'5422 Sampling site

1km

Fig. 1. Map showing the site of the accident and the area affected by the oil spill.

environmental contamination through biota using species with whereas crabs and barnacles were sampled at six fixed stations distinct ecological niches. This approach allowed an assessment (Fig. 1). Specimens were maintained in ice in an isotherm box until of environmental contamination from different perspectives, tissue extraction in the laboratory. Muscle tissue (10 g) of each col- allowing a better evaluation of the accident and its consequences. lected fish and crab was extracted and approximately 10 barnacles Guanabara Bay is one of the most important embayments of the were pooled per station in order to obtain enough mass for analy- Brazilian coast and various forms of pollution threaten its estuarine sis. Specimens of crabs and fishes from reference areas (Angra dos environment. The bay includes two refineries, 16 oil terminals, Reis and Itaipú) and from a fish market (São Pedro Municipal Mar- 6000 industries and two shipyards, and receives an estimated daily ket, Niterói) were also analysed for comparison. oil input around 9.5 tons, among other pollutants (Francioni et al., PAH extraction was carried out based on the extraction method 2005). The PAH contamination of the bay sediment was docu- employed by Meniconi et al. (2002). Each sample was freeze-dried mented by several studies (Hamacher, 1996; Lima, 1996; Meniconi and approximately 1 g of the homogenate was extracted in Tedia et al., 2002) and a detailed description of the bay has been pre- methylene chloride pesticide grade (50 mL) for 3 min, using a high sented by Kjerfve et al. (1997). In spite of being located in a highly rotation tissuemizer (11,000–16,000 rpm). The residue obtained urbanized area and thus considered heavily polluted (Kjerfve et al., was re-extracted and the extracts were pooled and filtered. The li- 1997), the bay supports important local fisheries (Jablonski et al., pid content was reduced by cleanup on a 2% deactivated Merck 2006) and still retains 90 km2 of fringing mangroves (Pires, 1992) aluminium oxide 90 active neutral (70–230 mesh ASTM) column of which ca. 50% are relatively preserved inside the Guapimirim (20 g), using 100 mL of methylene chloride. The extract obtained Environmental Protection Area (APA de Guapimirim). after cleanup was concentrated on a rotatory evaporator to 5 mL. After the oil spill, monthly samples were taken in the affected Fixed Fluorescence spectroscopy (FF) measurements were per- area. The first sampling was conducted between 6th and 10th days formed on a Perkin-Elmer LS 55 Luminescence Spectrometer. Spec- after the accident on May 2nd to 6th 2005. The second was also tra were recorded in 1 cm quartz cuvettes with both excitation (ex) carried out in May and after that, monthly samplings were per- and emission (em) slit widths set to 4 nm. Pyrene (>97%) pur- formed until March 2006, totalling 12 surveys. Each sampling sur- chased from Sigma (St. Louis, USA) was used as the standard PAH vey was performed within the affected area (i.e. were the oil slick and its optimal wavelength pair for detection was identified as was observed in the first campaign), and in each survey different being 334/383 nm. As other polycyclic aromatic compounds can species of fish, the crab Ucides cordatus and the barnacle Fistulobal- present fluorescent properties in the same wavelength pair used anus citerosum were collected. Fish were randomly collected, for detection, results were indicated as pyrene equivalents. The

A. Soares-Gomes et al. / Marine Pollution Bulletin xxx (2010) xxx–xxx 3

Table 1 the accident), in levels higher than those of the first sample after List of sampled fish from the oil exposed area. Frequency (f), relative frequency (F), the accident (May 2005a), decreasing again to lower concentra- abundance (A) and dominance (D, %). Names with an asterisk are those used in tions in February and March 2006. The values observed in January analysis. 2006 may be associated with the rainy season, when runoff from Species fF(%) AD(%) adjacent systems can expose the environment to another peak of Fishes oil exposure, not necessarily from the studied accident, as the Micropogonias furnieri (Desmarest, 1823)* 12 100 86 18.5 Caceribu basin drains water from at least four cities (Itaborai, Tan- Genidens genidens (Cuvier, 1829)* 12 100 65 14.0 gua, Rio Bonito and São Gonçalo) with approximately 300,000 Geophagus brasiliensis (Quoy and Gaimardi, 1824)* 11 92 79 17.0 Hoplostemum littorale (Hancock, 1828)* 11 92 47 10.1 inhabitants. Centropomus parallelus (Poey, 1860)* 10 83 49 10.5 From the eight selected fishes, two were top carnivors (Centrop- Hoplias malabaricus (Bloch, 1794)* 8 67 15 3.2 omus parallelus and Hoplias malabaricus), three benthic omnivorors Brevoortia aurea* 7 58 25 5.8 (Mugil liza, Geophagus brasiliensis and Genidens genidens), one Mugil liza (Valenciennes, 1836)* 6 50 17 3.7 Elops sauro (Linnaeus, 1766) 6 50 10 2.2 planktivorous (Brevoortia aurea) and two benthic carnivorors Clarias gariepinus (Burchell, 1822) 6 50 8 1.7 (Hoplostemum littorale and Micropogonias furnieri). The crab ( U. Cetengraulis edentatus (Cuvier, 1829) 5 42 28 6.0 cordatus) feeds on mangrove leaves and the barnacle (F. citerosum) Cathorops cf. spixii (Agassiz, 1829) 3 25 17 3.7 is a suspension feeder. The different diets did not reflect PAH con- Conodon nobilis (Linnaeus, 1758) 3 25 3 0.6 centrations since a similar pattern was observed for all species dur- Hypostomus affinis (Steindachner, 1877) 3 25 3 0.6 Centropomus undecimalis (Bloch, 1792) 2 17 5 1.1 ing the months after the accident. One could expect that the Oreochromis niloticus (Linnaeus, 1758) 2 17 2 0.4 different diets would exhibit particular contamination levels but Anchoa tricolor 1 8 3 0.7 this was not the case for the fishes studied in this investigation. Hoplerithynus unitaeniatus (Spix, 1829) 1 8 3 0.6 This fact might be correlated with the high level of inducible Total 465 MFO activity (cytochromes P450 mixed function oxygenase sys- tem) that is able to metabolize and excrete accumulated PAHs rap- Barnacle Fistulobalanus citerosum (Henry, 1973)* 12 100 50 100 idly (van der Oost et al., 2003). Alternatively, the low values observed in most fishes, regardless of their diet, may be associated Crab with their mobility or to the fact that most occur in the water col- Ucides cordatus (Linaeus, 1763)* 12 100 190 100 umn rather than the air–water interface, where most of the oil slick was located. Nonetheless, our results did not show consistent pat- terns of accumulation relative to the different diets of the fishes work range was 30–150 lgLÀ1, the limit of detection was collected. 8.274 lgLÀ1 and the limit of quantification was 25.15 lgLÀ1 for The barnacle F. citerosum was the most sensitive species to oil the diluted samples. exposure, being the only species with PAH values above A total of 465 specimens of fish from 18 species were collected, 100 lgkgÀ1 in the first two sampling periods after the spill (May from which eight were selected as the most representative due to 2005a and May 2005b); in the third survey (April 2005) the PAH their relative frequency (>50%) and abundance (>3%), accounting concentration levels were similar to the other species (Fig. 2). Bar- for 86% of the fish specimens collected (Table 1). Considering the nacles are sessile and F. citerosum lives in the low midlittoral zone sampling feasibility, 190 specimens of the crab (U. cordatus) and on mangrove roots exposed to contaminants without the possibil- 50 barnacle samples (F. citerosum) were collected. Monthly values ity of escaping. No mortality was observed for this species follow- of PAH concentrations obtained for each selected species are pre- ing the oil spill, and the values of PAH concentration observed for sented (Figs. 2–5). barnacles may as well be associated with its sessile habitat and Categorization of fish tissue contamination (after Varanasi et al., feeding mode. According to Neff (2002), burrowing and filter-feed- 1993) was used as a reference (Table 2). Nevertheless, as these ing shellfish species are more likely to accumulate PAHs from oil authors’ values were obtained utilising different techniques (GC/ spills than finfish because they are more vulnerable to exposure MS) than those here employed, the categorization was used with and less efficient at metabolizing petroleum compounds once ex- caution. For fish, all but January 2006 samples could be classified posed. These results are in accordance with those obtained by as minimally contaminated. A second contamination increase Francioni et al. (2005) for the GC/MS analysis of mussels collected was observed in the following summer months with a peak of con- after a major oil spill in Guanabara Bay in January 2000. A similar centration in almost every species of January 2006 (9 months after pattern was observed by Niyogi et al. (2001) for barnacles collected

-1 400 gktnelaviuqeenerypg Mean 350 ±SE 80 80 300 Mean Mean Fistilobalanus citerosum Brevoortia aurea ±SE Ucides cordatus ±SE 250 60 60 -1 50µg.kg 50µg.kg-1 200 40 40

µ)

(noitartnecnoC 150

100 20 20 4 -1 50 50µg.kg 43 44344 444 4 31 7 6 31 4 14 16 18 18 18 18 18 17 18 18 19

0 0

a50yam b50yam

b50yam

a50yam

a50yam b50yam

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50zed

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60ram

60vef

50tes

50tco

50tes

60vef

50von

50zed

50luj

60naj 50nuj

50tco

60vef 50tes 50luj

Fig. 2. PAH (pyrene equivalent lgkgÀ1) concentrations per month (from May 2005 to March 2006) of Fistulobalanus citerosum, suspension feeder barnacle; Brevoortia aurea, planktivorous ﬁsh; and Ucides cordatus, organic detritus feeder crab. Numbers of specimens for each month are displayed above the month’s label.

4 A. Soares-Gomes et al. / Marine Pollution Bulletin xxx (2010) xxx–xxx

120 160 Mean

-1 ±SE Mean

kg Hoplias malabaricus 140 Centropomus parallelus ±SE

nelaviuqeenerypg 100

120 80 100

60 80 -1 µ) 50µg.kg

(noitartnecno 60 -1 40 50µg.kg 40

20 Ct 20 1111113627722221 123

0 0

a50yam

b50yam

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60vef

50tes

50tco

50luj

50gua

50zed

50von

60naj

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50tco 50luj

Fig. 3. PAH (pyrene equivalent lgkgÀ1) concentrations per month (from May 2005 to March 2006) of Hoplias malabaricus and Centropomus parallelus, top carnivorous ﬁshes. Numbers of specimens for each month are displayed above the month’s label.

120 Mean Genidens genidens ±SE

)tn

-1 100

ela

viuqeenerypgµ 80 80 80 Mean Mean Geophagus brasiliensis ±SE Mugil liza ±SE 60 60 60 -1 50µg.kg-1 50µg.kg-1 50µg.kg

(noitartnecnoC

40 40 40

20 20 20

7 645 543112468 27104108279137 5 33 1 32

0 0 0

b50yam

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b50yam a50yam

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50-nuj

50-luj

feb-06

oct-05

aug-05 sep-05 nov-05 dez-05 mar-06

Fig. 4. PAH (pyrene equivalent lgkgÀ1) concentrations per month (from May 2005 to March 2006) of Genidens genidens, Geophagus brasiliensis and Mugil liza, benthic omnivorous ﬁshes. Numbers of specimens (when collected) for each month are displayed above the month’s label.

120

)tnelaviuqeenerypgµ -1 Mean

kg 100 Hoplosternum littorale ±SE

80 80 Micropogonias furnieri Mean ±SE 60 -1 60 50µg.kg 50µg.kg-1

(noit 40 40

artnecnoC

20 20 11 4 3 3 1 1 4 7 3 8 2 21 6 4 8 2 7 8 5 9 10 3 3

0 0

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50ced 50von

b50yam a50yam

oct 05 aug 05

Fig. 5. PAH (pyrene equivalent lgkgÀ1) concentrations per month (from May 2005 to March 2006) of Hoplostemum littorale and Micropogonias furnieri, benthic carnivorous ﬁshes. Numbers of specimens for each month is displayed above the month’s label.

in a PAH exposed site, with much higher concentrations than those Table 2 from a reference site. Fish tissue contamination criteria (adapted from Varanasi et al. (1993)). Immediately after the oil spill incident in Itaboraí, ICMBio insti- 1 Classiﬁcation PAH concentration (lgkgÀ ) gated a temporary closure of seafood harvesting in the area af- Not contaminated <10 fected by the spill and its surroundings (APA de Guapimirim). Minimally contaminated 10–99 This was a preventive measure in order to collect and evaluate Moderately contaminated 100–1000 information on the nature of the spill, such as oil type, fate, trans- Highly contaminated >1000 port and seafood resources at risk of exposure.

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Table 3 Values of PAH (pyrene equivalent lgkgÀ1) concentrations at reference sites.

Espécie Month n Average Range Std. deviation Ucides cordatus (crab) Brachuy, Angra dos Reis, RJ July/2005 3 23.3 17.6–33.0 8.2 Brachuy, Angra dos Reis, RJ September/2005 1 18.6 – – Mugil liza (fish) Itaipu, Niterói, RJ September/2005 3 26.4 23.2–31.9 4.8 São Pedro Fish Market, Niterói, RJ April/2006 3 23.6 9.8–41.0 15.9 Micropogonias furnieri (fish) Itaipu Beach, Niterói, RJ June/2005 3 17.1 12.5–19.8 4.0 São Pedro Fish Market, Niterói, RJ April/2006 3 15.7 11.0–39.5 15.7 Cetengraulis edentatus (fish) São Pedro Fish Market, Niterói, RJ April/2006 3 34.4 26.7–47.9 11.7 Centropomus parallelus (fish) São Pedro Fish Market, Niterói, RJ April/2006 1 12.4 – –

Samples from reference sites and the fish market were classified References as minimally contaminated, with values ranging from 9.8 to 47.9 lgkgÀ1 PHA (Table 3). The background levels of oil contami- Ariese, F., Beyer, J., Jonsson, G., Visa, C.P., Krahn, M.M., 2005. Review of Analytical Methods for Determining Metabolites of Polycyclic Aromatic Compounds nation in Guanabara Bay have not been established. It is expect (PACs) in Fish Bile. ICES Techniques in Marine Environmental Sciences, No. À1 that a background level would lie within the range 10–50 lgkg 39, Copenhagen, Denmark. based on samples from reference sites (Table 3) and from contam- Fleming, L.E.,Broad, K., Clement,A.,Dewailly,E., Elmir,S.,Knap, A.,Pomponi,S.A.,Smith, ination values observed in the following months after the accident, S., Gabriele, H.S., Walsh, P., 2006. Oceans and human health: emerging public health risks in the marine environment. Marine Pollution Bulletin 53, 545–560. À1 when values below 50 lgkg were found for the majority of spe- Francioni, E., Wagener, A., Scofield, A.L., Cavalier, B., 2005. Biomonitoring of cies (Figs. 2–5). This range is in line with Silva et al. (2007), where polycyclic aromatic hydrocarbon in Perna perna from Guanabara Bay, Brazil. values between 4 and 53 lgkgÀ1 PAHs were established for two Environmental Forensics 6, 361–370. Hamacher, C., 1996. Determinação de hidrocarbonetos em amostras de água e fish species from Guanabara Bay. This range is within the ‘‘mini- sedimento da Baía de Guanabara (in Portuguese, with English abstract). Master mally contaminated” level and the background level proposed Thesis, PUC-Rio, Brazil. herein might suggest that Guanabara Bay is under chronic oil Hoffman, D.J., 2003. Handbook of Ecotoxicology. CRC Press, Boca Raton, Florida. Jablonski, S., Azevedo, A.F., Moreira, L.H.A., 2006. Fisheries and conflicts in exposure. Guanabara Bay, Rio de Janeiro, Brazil. Brazilian Archives of Biology and According to Yender et al. (2002), diesel-like products show Technology 49 (1), 79–91. moderate to high risk of seafood contamination because of their Kjerfve, B., Ribeiro, C.H.A., Dias, G.T.M., Filippo, A.M., Quaresma, V.S., 1997. Oceanographic characteristics of an impacted coastal bay: Baía de Guanabara, relatively high content of low molecular weight, water-soluble aro- Rio de Janeiro, Brazil. Continental Shelf Research 17, 1609–1643. matic hydrocarbons, which are very volatile. In addition, they Lima, A.L., 1996. Geocronologia de hidrocarbonetos poliaromáticos (PAHs). Estudo evaporate slowly and dispersed droplets are also bioavailable. de caso: Baía de Guanabara, Rio de Janeiro (in Portuguese, with English abstract). Master Thesis, PUC-Rio, Brazil. However, whether seafood is exposed and contaminated not only Malins, D.C., McCain, B.B., Landahl, J.T., Myers, M.S., Krahn, M.M., Brown, D.W., Chan, depends on a series of weathering processes which determine S.-L., Roubal, W.T., 1988. Neoplastic and other diseases in fish in relation to toxic the bioavailability of contaminants but also physiological pro- chemicals: an overview. Aquatic Toxicology 11, 43–67. cesses which determine the extent of uptake and the extent to Meniconi, M.F.G., Gabardo, I.T., Carneiro, M.E.R., Barbanti, S.M., da Silva, G.C., Massone, C.G., 2002. Brazilian oil spills chemical characterization – case studies. which compounds are retained or metabolized. Environmental Forensics 3, 303–321. Fistulobalanus citerosum appeared to be highly sensitive to oil Neff, J.M., 2002. Bioaccumulation in Marine Organisms: Effects of Contaminants exposure and could be effectively used in assessing post-spill im- from Oil Well Produced Water. Elsevier, Amsterdam. Niyogi, S., Biswas, S., Sarker, S., Datta, A.G., 2001. Seasonal variation of antioxidant and pacts; along with a calibration with fish tolerance values, barnacles biotransformation enzymes in barnacle, Balanus balanoides, and their relation could be used as sentinel species for further oils spill monitoring, with polyaromatic hydrocarbons. Marine Environmental Research 52, 13–26. as has been suggested by Viñas et al. (2009). The species consid- Pires, I.O., 1992. Monitoramento dos manguezais da APA-Guapimirim através de correlação de dados da fitomassa e da radiância TM/Landsat. Ph.D. Thesis, ered in this survey are restricted to the estuarine intertidal zone, Universidade de São Paulo. and other intertidal species of barnacles could be selected in more Silva, T.F., Azevedo, D.A., Aquino Neto, F.R., 2007. Polycyclic aromatic hydrocarbons wave-exposed shores. in fishes and sediments from the Guanabara Bay, Brazil. Environmental Forensics 8, 257–264. As observed in this study, it was difficult to continuously sam- van der Oost, R., Beyer, J., Vermeulen, N.P.E., 2003. Fish bioaccumulation and ple most fish species in the months following the incident, and biomarkers in environmental risk assessment: a review. Environmental only five of 18 species were re-sampled over a 10 month period. Toxicology and Pharmacology 13, 57–149. Varanasi, U., 1989. Metabolism of Polycyclic Aromatic Hydrocarbons in the Aquatic This may be due to seasonality or low abundance, among other Environment. CRC Press, Boca Raton, Florida. reasons. In this kind of post-impact study, where little informa- Varanasi, U., Brown, D.W., Hom, T., Burrows, D.G., Sloan, C.A., Field, L.J., Stein, J.E., Tilbury, tion on species occurrence and abundance is available, the use K.L., McCain, B.B., Chan, S., 1993. Survey of Alaskan Subsistence Fish, Marine of feasible species is recommended and in this way crabs, barna- Mammal, and Invertebrate Samples Collected 1989–91 for Exposure to Oil Spilled from the Exxon Valdez, vol. 1. NOAA Technical Memorandum NMFS-NWFSC-12. cles and certain fish species are the best choice. Barnacles and Viñas, L., Franco, M.A., Soriano, J.A., González, J.J., Ortiz, L., Bayona, J.M., Albaigés, J., other sessile filter-feeding organisms have already been demon- 2009. Accumulation trends of petroleum hydrocarbons in commercial shellfish strated to be appropriate sentinel species (Viñas et al., 2009), from the Galician coast (NW Spain) affected by the Prestige oil spill. Chemosphere 75, 534–541. and in this work barnacles were efficient bioindicators in the Yender, R.J., Michel, J., Lord, C., 2002. Managing Seafood Safety after an Oil Spill. early stage of the impact, providing an adequate assessment of Seattle Hazardous Materials Response Division, Office of Response and the pollutant agent. Restoration, National Oceanic and Atmospheric Administration, 72p.