Validation of ucides_cordatus_as_a_bioindicator_of

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Validation of Ucides cordatus as a bioindicator of oil contamination and
bioavailability in mangroves by evaluating sediment and crab PAH records
Article  in  Environment International · May 2007
DOI: 10.1016/j.envint.2006.11.001 · Source: PubMed
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Validation of Ucides cordatus as a bioindicator of oil contamination
and bioavailability in mangroves by evaluating sediment
and crab PAH records
Adriana Haddad Nudi a
, Angela de Luca Rebello Wagener a,⁎, Eleine Francioni a,1
,
Arthur de Lemos Scofield a
, Carla B. Sette a
, Alvaro Veiga b
a
Departamento de Química, Pontifícia Universidade Católica do Rio de Janeiro, 22543-900 Rio de Janeiro, Brazil
b
Departamento de Engenharia Elétrica, Pontifícia Universidade Católica do Rio de Janeiro, 22543-900 Rio de Janeiro, Brazil
Received 6 July 2006; accepted 1 November 2006
Available online 6 December 2006
Abstract
This study is aimed at verifying the relevance of Ucides cordatus as a bioindicator of oil contamination and PAH bioavailability in mangrove
sediments. For this, crabs and sediment cores were sampled from five mangroves, including an area suspected of contamination derived from an
MF380 oil spillage, and analyzed for the 16 PAH in the USEPA priority list as well as for the five series of alkylated homologues. Concentrations
in sediments varied from 35 μg kg−1
in the lower core layer of the control area to 33,000 μg kg−1
in the upper layer of the most contaminated area.
Total PAH contents in crabs varied from 206 to 62,000 μg kg− 1
and were closely correlated to that in sediments. In general, individual PAH
profiles in both matrices were in good agreement. Phenanthrenes, however, were more predominant in crabs making up to 30–46% of the Total
PAH. Accumulation factors found in the range of 0.7 to 35 were highly variable even after normalizing concentrations for organic carbon and lipid
content. Survival in highly contaminated environment and reliable record of environmental contamination in the tissue provide evidence that
U. cordatus is an excellent bioindicator for oil in mangroves.
© 2006 Elsevier Ltd. All rights reserved.
Keywords: Ucides cordatus; Crabs; PAH; Oil contamination; Sediments; Monitoring
1. Introduction
The majority of Brazilian oil production derived from
offshore fields, mainly from the Campos Basin, in the state of
Rio de Janeiro. This area supplies nearly 80% of the oil
exploited in the country. The oil produced is transported,
transferred and/or processed in coastal areas, often populated
with mangrove forests which have been threatened by oil spills
and illegal oil releases. There is a need to develop adequate
means to monitor oil derived contaminants in these ecosystems,
as well as their effects on the mangrove distinctive biota. The
polycyclic aromatic hydrocarbons (PAH) present in oils are of
special concern because many of its constituents are persistent,
toxic and show mutagenic activity.
PAH are widely disseminated in aquatic environments as a
result of natural and anthropogenic processes. Petroleum,
incomplete combustion of fossil fuels (Neff, 1979) and forest
fires are important sources of this group of substances. PAH
from pyrolytic sources are predominantly non-substituted
parental polyaromatic hydrocarbons, while those present in
oils are largely alkylated homologues (Steinhauser and Boehm,
1992). Several papers have shown that marine organisms are
prone to bioaccumulate these substances, particularly in lipid-
rich tissues (Neff, 2002; Carls et al., 2004; Francioni et al.,
2005; Dugan et al., 2005).
PAH present in sediments or food are assumed to be less
bioavailable than in water, because bioaccumulation seems to
involve release in solution before uptake (Pruell et al., 1987).
The bioaccumulation of certain PAH by organisms in sediments
Environment International 33 (2007) 315–327
www.elsevier.com/locate/envint
⁎ Corresponding author. Tel.: +55 21 3527 1809; fax: +55 21 2239 2150.
E-mail address: angela@rdc.puc-rio.br (A. de Luca Rebello Wagener).
1
Present address: Laboratório de Química Ambiental, PETROBRAS/
CENPES/PDEDS/AMA, 21941-598 Rio de Janeiro, Brazil.
0160-4120/$ - see front matter © 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.envint.2006.11.001

depend, therefore, on their water solubility, water/solid phase
partitioning and Kow (Bierman, 1990; Lamoureux and Browna-
well, 1999), as well as on the solid phase properties, as for
instance, organic carbon content and speciation (Rust et al.,
2004; Sundelin et al., 2004; Cornelissen et al., 2005). Crus-
taceans and bottom dwelling organisms can absorb toxics by
ingesting contaminated food. Biotic (reproductive stage, age,
sex, metabolism, lipid content, etc.) and physical (temperature
and salinity) factors also influence bioaccumulation (Meador
et al., 1995; Neff, 2002) and are responsible for the concen-
tration variability observed within a population.
Organisms that accumulate contaminants but are resistant to
their toxicity can be used in monitoring contamination in the
marine environment (Cossa, 1989). Among various aquatic
organisms, invertebrates have been preferred for environmental
assessment. They are the major components in all ecosystems
and, because of the usually numerous population, they can be
sampled for analyses with little damage to population dynamics
(Depledge and Fossi, 1994). Mussels are most frequently used as
biomonitors of water contamination because of the abundance,
resilience, and high bioaccumulation of several contaminants of
concern. Bioaccumulation of PAH in contaminated sediments by
crab species has been reported (Pancirov and Brown, 1977;
Hellou et al., 1994; Kayal and Connell, 1995; Axys Group,
1995; Baumard et al., 1998; Eickhoff et al., 2003; Dugan et al.,
2005). Nevertheless, very few address bioaccumulation of al-
kylated homologues and none of these reports target the
validation of crabs as a biomonitor for oil contamination.
Also, there are no reports of monitoring oil contamination in
mangrove ecosystems by using crabs.
Crabs are more efficient than mussels in biotransforming
PAH into polar metabolites, facilitating excretion (Fillmann
et al., 2004). The crab hepatopancreas plays a role similar to the
liver in vertebrates and is the organ where biotransformation
takes place. Therefore, analyses of contaminants in hepatopan-
creas provide information primarily on recent exposure and
should reflect actual levels in the environment.
The crab Ucides cordatus is ubiquitous in inter-tidal habitat
along the Brazilian coast. In mangroves, during low tide,
U. cordatus escapes to sediment burrows where it can be direct-
ly exposed to contaminants deposited in this environment. Such
a species is a good candidate to be used as biomonitor for PAH
contamination in mangroves which are among the ecosystems
most vulnerable to oil contamination (Grundlach and Hayes,
1987).
Once an oil spill reaches a mangrove, degradation is slow and
forest restoration may take several decades (Tam et al., 2001). The
persistence of oil in mangrove sediments is also associated to the
activity of crustaceans by which the contaminant may be carried
down to lower layers of the sediment, where degradation is slow
due to reduced molecular oxygen concentrations. According to
Irwin et al. (1997) this effect is more significant for the high
molecular weight PAH. It is recognized that the fate of oils in
mangrove and the associated impact will vary for different oils
and depends on the properties of the mangrove area.
The goal of the present study was to investigate the
suitability of U. cordatus as a biomonitor of oil contamination
in mangrove sediments and as an indicator of oil bioavailability.
For this, PAH concentrations as well as individual distribution
in crab tissue (hepatopancreas) and in sediments were obtained
and compared, as a means to determine: (1) the degree of
proportionality between environmental contamination and body
burden; and (2) how closely crabs reproduce PAH source
fingerprinting found in sediments. This work also aimed to
determine PAH levels in a mangrove contaminated by a major
oil spill that took place in January 2000 in Guanabara Bay.
2. Materials and methods
2.1. Study area
Guanabara Bay is an urban estuary surrounded by a densely populated area of
the city of Rio de Janeiro and of other seven smaller municipalities. This bay was
selected to test the possibility of using U. cordatus as a biomonitor for oil in
mangrovesedimentsowingto: (1) the presence of mangrove forests,some of which
were contaminated in January 2000 by a major spill of MF 380 oil; (2) the presence
of several potential oil sources (two oil refineries, an oil terminal, the second largest
harbor in the country, several ship yards and marinas, intense ship traffic, urban
runoff, oil transport and transfer); (3) the role played as a service area to the oil
exploitation fields in Rio de Janeiro, providing infrastructure and ancillary
activities for the petroleum industry.
2.2. Sampling
The strategy was to obtain sediment cores and crab samples from mangrove
areas in Guanabara Bay thought to have different PAH contamination levels.
Sediments and crabs were collected from five mangrove areas (Fig. 1). Four
areas are in Guanabara Bay (Peteca Channel (PT) sampled in 2004; Nova
Orleans (NO); Surui (S); and Piedade (P) sampled in 2003 and 2004) and one,
taken as control, is in Guaratiba (G, sampled in 2004). Guaratiba is a rather
pristine area located 60 km west of Guanabara Bay (Fig. 1). The Surui
mangrove, situated between two branches of the Surui River, is frontally and
laterally flooded during high tide. In all mangrove areas, except for Piedade,
cores and crabs were collected at two stations: station 1 was near the fringe,
where higher contamination levels were expected; and station 2 was located
about 200–300 m inland from the fringe. In the Peteca, station 1 is in a site
crisscrossed by underground oil pipelines while station 2 is at the bay rim.
Sediment samples (S) were collected by using a piston corer (Husky Duck
Equipments) especially devised for sampling mangrove sediments and equipped
with 1.0×0.07 m sharp edged aluminum tubes. In each station samples were taken
from 5 different points located 10 m apart. A total of five cores were then available
at each station. Each core was sliced into three layers labeled as: layer 1: 0–28 cm;
layer 2: 28–58; and layer 3: 58–90 cm. Thereafter, sediment layers from
corresponding depths were mixed together to produce three composite samples for
each station. The thicknesses of the first two layers were defined based on the depth
intervals from where crabs were collected. Crabs were usually harvested from
burrows up to 40–50 cm deep. In spite of this, a sediment layer below this depth
was sampled to cautiously check for possible influences of the PAH content on the
crabs. Cores from Guaratiba and Peteca had shorter lengths and were sliced into
two layers of 0–28 cm and 28–58 cm. Samples were stored in clean aluminum
boxes at −20 °C. A separate set of cores was used to measure pH, Eh (redox
potential) and to sub-sample for organic carbon, grain size and water content
determinations as described in Section 2.3.
Crabs were collected from the same sites as for sediments with the help of
artisan fishermen. The number of harvested crabs varied from 15 to 30 as a result
of the availability at each site. Animals were removed manually from the
burrows and only adult males with carapace size in the range of 60–70 mm were
taken. Females were not sampled to avoid the uncertainties imposed by the
reproductive cycle. In the laboratory, mud was removed from each animal before
weighing and measuring the carapace width with vernier calipers. Hepatopan-
creas (H) were removed with the help of surgical tools (decontaminated with
detergent, acetone and dichloromethane) after opening the carapace with
scissors. The material collected from the set of 15–30 crabs was lumped together
316 A.H. Nudi et al. / Environment International 33 (2007) 315–327

before homogenization in an UltraTurrax (Ika Labortechnik-T25 basic), and
storage in clean glass containers at −20 °C. Sub-aliquots for lipid content and
dry weight determination were stored separately.
2.3. Determination of ancillary data in sediment
Eh and pH were measured in fresh sediments, immediately after sampling,
with a platinum electrode and a combined glass electrode, respectively.
Sediment fraction b63 μm was determined gravimetrically after treating the
samples with hydrogen peroxide, drying and sieving through a 63 μm sieve.
Organic carbon determination was performed in 10 mg aliquots of the 63 μm
fraction, after eliminating carbonates with 2 M HCl (Suprapur Merck) and
drying at 60 °C to constant weight. Measurements were carried out in a TOC-
5000A Shimadzu equipped with an SSM-5000A module for solid samples.
Water content was determined gravimetrically.
2.4. Determination of PAH in sediments
PAH determinations were based on the USEPA (US Environmental Protection
Agency) methods 3540C (USEPA, 1996a) and 8270C (USEPA, 1996b). Aliquots
of 10 g of fresh sediment were treated with anhydrous Na2SO4 (Merck) previous-
ly decontaminated at 450 °C. To this mixture, 100 ng of p-terphenyl-d14
(AccuStandard) were added as surrogate standard before Soxhlet extraction over
24 h with a 1:1 mixture of dichloromethane-acetone (UltimAR-Mallinckrodt). The
extract was rotary evaporated and concentrated to about 1 mL under gentle stream
of purified N2, prior to solvent exchange to hexane (UltimAR-Mallinckrodt).
The aromatic fraction was cleaned and separated in a glass column (1.3 cm i.d.
and 30 cm height) packed in the top with colloidal copper for sulfur removal,
followed by 1 g of anhydrous Na2SO4, 1 g of alumina (Merck) 2% water
deactivated, and 11 g silica gel (Merck, 230–400 mesh) activated at 160 °C.
PAH were eluted with 50 mL of a 1:1 hexane-dichloromethane (UltimAR-
Mallinckrodt) mixture. The aromatic fraction was then rotary evaporated and
concentrated under nitrogen stream before quantitative transference to a 1 mL
class A volumetric flask. The volume was completed with hexane after adding
100 ng of an internal standard mixture containing naphthalene-d8,
acenaphthene-d10, phenanthrene-d10, chrysene-d12 and perylene-d12
(AccuStandard).
2.5. Determination of PAH in hepatopancreas
PAH determination in the hepatopancreas homogenates was performed in
triplicate according to the procedure described below.
To aliquots of 3 g of tissue homogenate, 30 g anhydrous Na2SO4 previously
decontaminated at 450 °C were added followed by 100 ng of p-terphenyl-d14,
used as surrogate standard. The mixture was Soxhlet extracted with 200 mL
dichloromethane over 24 h. The obtained extract was rotary evaporated and
concentrated to approximately 1 mL under N2 stream. The 70% lipid content in
the extracts were reduce in two steps: (1) the extract was first cleaned by
adsorption chromatography in a 2.2 diameter×30 cm length glass column
packed with 20 g of 2% deactivated neutral alumina. After elution with 100 mL
of dichloromethane, the extract was rotary evaporated and concentrated under
N2 stream to approximately 1 mL before solvent exchange to acetone-
cyclohexane (3:7) (HPLC/Spectro, Tedia); (2) the pre-cleaned extract was
further purified by gel permeation using a Shimadzu system equipped with a
LC-10AD pump, a UV–VIS detector Shimadzu and Shodex CLNpack columns.
Acetone-cyclohexane was used for eluting the analytes of interest. The elution
volumes where calibrated with a GPC EPA mixture (AccuStandard) containing
corn oil, bis(ethylhexyl) phtlalate, methoxychlor, perylene and sulfur. The
purified extract was rotary evaporated and concentrated under gentle N2 stream
to about 1 mL. After volume correction the extract was treated as described in
item 2.4 to obtain the aromatic fraction.
2.6. GC-MS analysis, quantification and quality assurance
Determination using a full scan mode proceeded in a Finnigan Trace GC gas
chromatograph coupled to a Finnigan Polaris Q Ion Trap mass spectrometer fitted
with a J and W DB-5 MS.ITD capillary column (30 m×0.25 mm×0.25 μm).
Helium, the carrier gas, was adjusted at 1.2 mL min− 1
and the column
Fig. 1. Location of the sampling sites in the Guanabara Bay (Piedade (P), Nova Orleans (NO), Surui (S), Peteca (PT)) and in Barra de Guaratiba (G), the control area.
317A.H. Nudi et al. / Environment International 33 (2007) 315–327

temperature was programmed as follows: 5 min at 50 °C, 50 °C min− 1
up to
80 °C, 6 °C min− 1
from 80 °C to 280 °C, and a final hold of 25 min at 280 °C. The
injector temperature was at 250 °C (interface at 300 °C and ion source at 250 °C;
electron impact 70 eVand emission current 250 mA), and the injected volume in
splitless mode was 2 μL.
Quantification included the following 37 compounds and/or groups of
alkylated compounds: (1) The 16 USEPA PAH: naphthalene (N), acenaphthy-
lene (Acen), acenaphthene (Ace), fluorene (F), phenanthrene (Ph), anthracene
(Ant), fluoranthene (Fl), chrysene (Ch), pyrene (P), benzo(a)pyrene (BaP), benz
(a)anthracene, (BaAnt), benzo(b)fluoranthene (BbFl), benzo(k)fluoranthene
(BkFl), indeno(1,2,3-c,d)pyrene (IP), dibenz(a,h)anthracene (DBAnt), benzo
(ghi)perylene (BghiPe); and (2) perylene (Pe), dibenzothiophene (DBT), benzo
(e)pyrene (BeP), alkylated naphthalenes (C1N, C2N, C3N and C4N), fluorenes
(C1F, C2F and C3F), phenanthrenes (C1Ph, C2Ph, C3Ph and C4Ph),
dibenzothiophenes (C1DBT, C2 DBT and C3DBT), chrysenes (C1Ch and
C2Ch) and pyrenes (C1P and C2P).
Standard solutions in two concentration ranges were used for quantification:
one for the low concentration levels (5, 10, 20, 50, 100 ng mL− 1
) and another for
the higher concentration levels (50, 100, 200, 400 and 1000 ng mL− 1
). They were
prepared including 100 ng mL− 1
of each deuterated standard (naphthalene-d8,
acenaphthene-d10, phenanthrene-d10, chrysene-d12 and perylene-d12), the 16
USEPA PAH, 2-methylnaphthalene, 1-methylnaphthalene, dibenzothiophene,
and pyrene (AccuStandard). Quantification of the alkylated PAH was based on
the calibration curve of the non-alkylated homolog except in the case of 1 and 2
methyl-naphthalene, for which authentic standards were available. Baselines for
the alkylated PAH were set manually. Linear correlation coefficients N0.990 were
obtained for the calibration curves in all cases. For each group of 10 analyzed
samples a standard solution of the above compounds was injected in the CG/MS
to verify instrumental calibration conditions. For each batch of samples at least
one analytical blank was analyzed.
For sediments, average recoveries of 71–110% (85±11%; n=39) were
obtained for p-terphenyl d14, the surrogate standard added to samples before
the extraction. As recommended in the EPA method, surrogate recovery was
not used to adjust analyte concentrations. Accuracy was checked by analyzing
the NIST 383 sediment reference material. Found values fell within the
expected range for all certified compounds except for naphthalene for which
recovery was low (30%). The quantitative limit for each PAH was 1 μg kg− 1
d.
w. and the detection limit (USEPA, 2002) for the dibenz (a,h) anthracene, a
compound that showed the lowest signal/noise ratio among all determined
PAH, was equivalent to 0.1 μg kg− 1
d.w. of sediment. Standard deviations
were below 10%.
For the hepatopancreas, recoveries of the surrogate standard were between 64
and 105% (75±21; n=55); the quantitative limit for each PAH was 3.5 μg kg− 1
d.w. and the detection limit was 0.7 μg kg−1
d.w. The relative standard deviation
of each individual compound in real samples ranged from 5.1 to 22% (n=5). The
quality assurance procedure included also the determination of PAH in fish tissue
reference material IAEA 406. The lowest recovery of 75% in relation to the
reference range was obtained for naphthalene. For all the other compounds
recovered concentrations were in the expected range.
2.7. Statistical evaluation
Factor analysis was performed as an exploratory analysis for the data set
obtained. For this the SPSS 8.0 program was used and the Varimax rotation with
Keiser normalization was selected to represent the planar projection of the two
first principal components. Spearman correlation test was used to search for
correlations (STATISTICA 6.0).
3. Results and discussion
3.1. PAH in sediments
The sediments contained 35 to 60% humidity, and 1.2 (Guaratiba) to
8.4% (Peteca and Nova Orleans) organic carbon (Corg). Among the
mangroves of Guanabara Bay, the Surui showed the lowest values for
both variables as well as the smallest fraction of fine sediments (fraction
b63 μm: Surui, 20–60%; Piedade, Nova Orleans and Peteca, 70–98%;
Guaratiba, 50–80%). As expected, Corg decreased with depth in the
sediment cores. As for pH and Eh, most samples from the first sampling
period were slightly anoxic (Eh around 0 Vup to −0.150 V) or oxic (Eh of
0.700 V in Peteca, for example) and pH was 6.86±0.52. In the second
sampling period pH was 6.78±0.18.
Sediments layers from Guanabara Bay mangroves showed a wide
range of PAH concentration (Table 1). In the upper sediment layer the
Total PAH ranged from 615 μg kg− 1
in Piedade to 33,000 μg kg−1
in Surui, while in Guaratiba (the control area) it was 175 μg kg−1
(Table 1).
The nonparametric Spearman test used to verify possible correla-
tions among PAH concentrations, pH, Eh and organic carbon gave
negative results. The lack of correlation between PAH and Corg can be
explained assuming that phase distribution of such compounds is
effectively controlled by specific fractions of Corg, as for instance black
carbon and humic material (McCroddy et al., 1996; Gustafsson et al.,
Table 1
PAH concentrations in sediment and hepatopancreas of Ucides cordatus from mangroves in Guanabara Bay and Guaratiba
Hepatopancreasa
Sediments
(0–28 cm) (28–58 cm) (58–90 cm)
Date Mangroves Sampling stations Total PAH Σ16 PAH Total PAH Σ16 PAH Total PAH Σ16 PAH Total PAH Σ16 PAH
(September 03) Piedade 1 303±87 85±14 615 305 658 366 312 153
Nova Orleans 1 6551±363 445±81 1135 234 671 292 275 46
2 925±82 58±4 1098 217 385 143 387 59
Surui 1 62297±6314 2290±773 31500 1001 22577 873 11618 509
2 62398±8291 1744±247 33082 913 9920 306 4556 480
(October 04) Piedade 1 330±27 41±4 792 421 352 132 379 116
Nova Orleans 1 2319±172 187±41 924 171 238 72 181 30
2 2056±177 117±3 1446 268 542 163 294 59
Surui 1 46272±3209 1519±39 23540 972 1358 188 1278 117
2 3316±81 164±13 6601 320 2859 229 667 62
Guaratiba 1 412±45 84±14 243 42 223 22 – –
2 206±33 26±4 175 22 34 10 – –
Peteca 1 4131±690 386±37 6132 630 1725 211 – –
2 5727±391 516±46 2550 337 592 92 – –
Total PAH and Σ16 PAH are given in μg kg− 1
dry weight.
a
Standard deviation for the hepatopancreas analysis in triplicate.

1997; Accardi-Dey and Geschwend, 2002), which may be present in the
studied sediments as different proportions of total Corg. These fractions
were not quantified in the present work.
The mangroves inGuanabara Bay can be ranked according tothe PAH
contamination level as follows: SuruiNPetecaNNova OrleansNPiedade.
Satellite images obtained after the oil spill of January 2000 demonstrated
that Peteca, in the proximity of the oil spill, and especially Surui had been
severely contaminated (Bentz and Miranda, 2001). The high concentra-
tions found three to four years after the spill in Surui provide indications
of the oil persistence in the mangrove as will be shown later.
In layers 1 and 2 of both Surui stations, alkylated naphthalenes
(ΣC1N=15,700 μg kg−1
; ΣC2N=14,500 μg kg−1
), alkylated pyrenes
(ΣC1P=3000 μg kg−1
; ΣC2P=2000 μg kg−1
), alkylated phenanthrenes
(ΣC1Ph=4700 μg kg−1
; ΣC2Ph=2300 μg kg−1
), alkylated fluorenes
(ΣC1F=3200 μg kg−1
; ΣC2F=1500 μg kg−1
) and alkylated chrysenes
(ΣC1Ch=2000 μg kg−1
; ΣC2Ch=1100 μg kg−1
) are the major
components, as should be expected for sediments contaminated with
oil. A decrease in concentration with depth is generally observed though
more accentuated in station 2 (Fig. 2) in 2003. At the fringe, tidal inflow
added to crustacean activity may contribute to downward transport of
Fig. 2. PAH distribution in sediment from Surui mangrove sampled in: September 2003 at station 1 (S11) and station 2 (S12), October 2004 at station 1 (S21) and
station 2 (S22). Layers 1 (0–28 cm), 2 (28–58 cm), and 3 (58–90 cm). PAH concentration in μg kg−1
d.w. Abbreviations: N (naphthalene); C1N–C4N (C1
naphthalene–C4 naphthalene); ACE (acenaphthylene); ACEN (acenaphthene); F (fluorene); C1F–C3F (C1 fluorene–C3 fluorene); Ph (phenanthrene); C1Ph–C4Ph
(C1 phenanthrene–C4 phenanthrene); Ant (anthracene); Fl (fluoranthene); P (pyrene); C1P–C2P (C1 pyrene–C2 pyrene); BaAnt (benz[a]anthracene);Ch (chrysene);
C1Ch–C2Ch (C1 chrysene–C2 chrysene); BbFl (benzo[b]fluoranthene); BkFl (benzo[k]fluoranthene); BaP (benzo[a]pyrene); BeP (benzo[e]pyrene); Pe (perylene);
IP (indeno[1,2,3-cd]pyrene); DBAnt (dibenz[ah]anthracene); BghiP (benzo[ghi]perylene); DBT (dibenzothiophene); C1DBT–C3DBT (C1 dibenzothiophene–C3
dibenzothiophene).

contaminants, leading to the high PAH concentrations observed in
sediments from 58–90 cm depth (11,600 μg kg−1
station 1, first
sampling).
In Surui, Total PAH declined from 2003 to 2004 in all sediment
layers of both stations 1 and 2. In layer 1 the decrease was of 75%.
As shown in Fig. 2, the increasing concentration of naphthalene and
fluorene homologues from C0 to Cn is typical of weathered oil.
Phenanthrenes and dibenzothiophenes in layer 1, however, show
predominantly bell-shaped concentration profiles, usually an indication
of recent oil inputs. The ratios C2DBT/C2Ph and C3DBT/C3Ph were
then used to investigate the source of the oil residues present in these
sediments. Such ratios are considered robust tools (Wang et al., 1999;
Readman et al., 2002) to identify the source of oils present in sediments.
The C2 pair, as well as the C3 pair, shows similar solubility and
weathering rates, which cause the concentration ratio to remain constant
in time. The calculated ratios for sediments from the two upper layers of
stations 1 and 2 in Surui (0.53bC2DBT/C2Phb0.65; 0.53bC3DBT/
C3Phb0.58) are similar to those of the MF380 oil (C2DBT/
Fig. 3. PAH distribution in sediment from mangrove Peteca mangrove sampled in: September 2003 at stations 1 (PT11) and station 2 (PT12), and in Guaratiba
mangrove (control area) at station 1 (G11) and station 2 (G12). Layer 1 (0–28 cm) and layer 2 (28–58 cm). PAH concentration in μg kg−1
d.w. (see Fig. 2 for
abbreviations).

C2Ph=0.59; C3DBT/C3Ph=0.64), in spite of the chronic oil
contamination in the bay (derived from illegal releases and frequent
spillage of diverse magnitudes), which interferes with the process of
identification of a single event. In the deeper sediment layers such
association is less straightforward, possibly due to the lower
contributions of MF380 to the mixture of earlier contaminations.
In light of the above results, the bell-shaped concentration dis-
tribution of Ph and DBT homologues may be ascribed to a relatively
higher persistence of these compounds in the mangrove environment.
The sandy acidic soil in Surui (among the studied areas only with
less than 35% of fine grains in surface sediments) may contribute to
stagnation of pollutant concentration.
Absorption inside organic particles or occlusion in other sediment
components may render the contaminants inaccessible to bacteria
responsible for degradation. Under these conditions half lives turn out
to be longer than expected for degradable substances. The formation of
tar droplets with low surface to volume ratios, that occurs in the case of
massive contamination, also limits the bacteria access to the PAH.
Also, it has been shown that the sequential metabolism of PAH by
marine microorganisms leads to preferential utilization of substrates.
For instance, Foght et al. (1989), and Stringfellow and Aitken (1995)
observed that naphthalene (N) undergoes preferential biodegradation in
comparison to phenanthrene (Ph); the presence of fluorene (F) also
retards Ph degradation. An attempt to verify possible hindrance of
Fig. 4. PAH distribution in sediment from Nova Orleans mangrove sampled in: September 2003 at station 1 (NO11) and station 2 (NO12); in October 2004 at station 1
(NO21) and station 2 (NO21). Layer 1 (0–28 cm), layer 2 (28–58 cm), and layer 3 (58–90 cm). PAH concentration in μg kg− 1
d.w. (see Fig. 2 for abbreviations).

phenanthrene degradation by these compounds was made here by
searching for trends between phenanthrene (ΣPh) and naphthalene
(ΣN)+fluorene (ΣF) concentrations. The Spearman test gave good
correlation coefficients for log ΣPh versus log (ΣN+ΣF) in Surui
(r2
=0.835; pb0.05; n=12) and also when grouping all examined
mangrove areas (r2
=0.882; slope of 0.85; pb0.05; n=26). The
possibility that these trends represent an in situ evidence of inter-
dependent PAH degradation must be better investigated. However they,
in principal, cannot be ascribed to a common origin of the compounds,
since the degradation rates of each single PAH considered separately
differ significantly and, therefore, should cancel out such correlations.
As for the differences in total concentration found in 2003 and
2004 (Table 1) degradation may not be the only cause, but they may
rather result from the combination of two factors: the difficulty in
positioning with high accuracy the sampling stations under the
mangrove forest, and the heterogeneous distribution of the oil in
sediments. In some cores, droplets of oil were visibly present and
may have contributed to the higher values in the 2003 sampling,
despite the use of sediment homogenate prepared using 5 cores from
each sampled station. This aspect underlines the complexity
associated with environmental impact assessment in mangrove
areas. It should be emphasized, however, that individual PAH
composition found in sediments collected in 2004 concurs with
those obtained for samples from 2003 (Fig. 2).
The Total PAH concentration found in Surui three to four years after
the oil spill is of the order of magnitude of those reported for sediments
from Caribbean coast mangrove in Bahia de Las Minas four years after
the Galeta Oil Spill (Burns et al., 1994) and from Prince William Sound
after the Exxon Valdez spill (O'Clair et al., 1996). Comparison with
other regions, as for instance those given under Readman et al. (2002),
is difficult because many of the cited reports address only parental PAH
which in the present case are not the prominent components.
Individual PAH distribution in Peteca (Fig. 3) differs from that in
Surui. The major compounds are alkylated phenanthrenes, pyrenes and
chrysenes, while naphthalenes are at the level of some tens of μg kg−1
.
The distribution profile of homologues indicates that oil residues are
further degraded than in Surui. Peteca has a known history of oil
contamination due to pipeline leakages and other events. This may
have resulted in adaptation of the microbial community to degrade oil
more effectively than in other examined mangroves. In spite of the
degradation and of the presence of other oil residues, samples from
station 2 show indicative ratios (C2DBT/C2Ph=0.62; C3DBT/
C3Ph=0.61) similar to those of MF380.
The Nova Orleans mangrove showed PAH concentrations more
than one order of magnitude lower than in Peteca or Surui. As shown in
Fig. 4, phenanthrenes are dominant in the first layer (from Ph=8.3 to
maximum in C3Ph=150 μg kg−1
) and the relative proportion of
dibenzothiophenes is higher than in the other stations, in all sediment
segments.
In Piedade (Fig. 5), the least contaminated mangrove in Guanabara
Bay, the individual PAH profile differs significantly from the others by
showing predominance of PAH heavier than fluoranthene. Guaratiba,
the control area, also shows a distinct individual PAH profile (Fig. 3) in
which naphthalenes, fluorene and pyrenes are dominant.
The ratio between the 16 USEPA PAH and the Total PAH can be
used to compare sources of hydrocarbon contamination, as high
proportions of parent aromatic hydrocarbons are characteristic of
pyrogenic residues. In Nova Orleans, in the intermediate sediment
layer, the significant contribution of heavier PAH of pyrolytic origin
leads to a rise in the Σ16 PAH to 50% of the total (Fig. 6). In Piedade,
the presence of quasi even proportions of petrogenic and pyrolytic PAH
is evident since the ratio of Σ16 PAH/Total PAH ranges from 49–56%,
in 2003, and from 30 (in the lowest segment)–53% in 2004. It should
be noted that combustion sources are abundant in the surroundings of
all mangrove areas (vehicles and industrial activities are most relevant
in the area of Peteca, while biomass burning is more important in the
other mangroves). However, combustion derived PAH was generally
low in sediments and in crab tissue. The contribution of Σ16 PAH to
Total PAH increased with decreasing contamination level; therefore, it
is less prominent in Surui and Peteca as shown in Fig. 6.
Besides the fraction of Σ16 PAH, there are at least four diagnostic
ratios usually applied to distinguish petrogenic sources from pyrolytic
Fig. 5. PAH distribution in sediment from Piedade mangrove sampled in: September 2003 (P11) and October 2004 (P21) at station 1. Layer 1 (0–28 cm), layer 2
(28–58 cm), and layer 3 (58–90 cm). PAH concentration in μg kg− 1

sources (Wang et al., 1999; Readman et al., 2002), such as: Ph/Ant, Fl/P,
C1Ph/Ph; and the Σother 3–6 rings PAH/Σ 5 alkylated PAH series (Σ5
alkylated PAH: C0–C4 naphthalenes and phenanthrenes; C0–C3
fluorenes and dibenzothiophenes; and C0–C2 chrysenes. Σother 3–6
rings PAH: other parental PAH with 3 to 6 rings plus perylene and benzo
(e)pyrene). Because chrysene and anthracene were not found in many
samples, only two ratios were applied here: Fl/P and “Σother 3–6 rings
PAH/Σ 5 alkylated PAH series”. Table 2 shows the results of these two
diagnostic ratios confirming predominance of petrogenic sources in
Surui. However, for Peteca, Nova Orleans, and Guaratiba (layer 1) only
Fl/P indicated petrogenic predominance. The diagnostic ratios indicate
inputs from both sources in Piedade.
The sediment quality benchmarks proposed by Buchman (1999) were
used to evaluate the potential risk of the measured PAH concentrations to
the benthic biota. In spite of the low fraction of priority USEPA PAH, in
Surui several of the 16 PAH were above TEL (Threshold Effect Level): in
station 2, acenaphthene was above PEL (Probable Effect Level=88.9 μg
kg−1
) and anthracene was close to the PEL (245 μg kg−1
); in stations 1
and 2, benz(a)anthraceneNTEL (88.81 μg kg− 1
), chryseneNTEL
(107.77 μg kg−1
), fluoreneNTEL (21.17 μg kg−1
), 2-methylnaphthale-
neNTEL (20.21 μg kg−1
). In Peteca benz(a)anthracene was also above
TEL. The sum of the low molecular weight PAH (N, Acen, Ace, F, Ph and
Ant) was above TEL (311.7 μg kg−1
) in the sediments of layers 1 and 2 of
station 1, and above ERL (552 μg kg−1
) in layer 1 of station 2. For the
sum of high molecular weight PAH (Fl, P, BaAnt, Ch, total BFl, BaP, IP,
DBAnt and BghiPe) only in layer 1 of station 1 the value was higher than
TEL (655.34 μg kg−1
). Benchmarks for alkylated homologues are not yet
available, although non-planar PAH seem to be more susceptible to react
in a biological system. Furthermore, the most important analytes to
consider in damage assessment for oil spills are the alkylated
homologues, which are more persistent and often more toxic than the
parental compounds (Sauer and Boehm, 1991; Irwin et al., 1997).
3.2. PAH in crabs
Weight and carapace length of sampled crabs ranged from 114 to
173 g and from 62 to 73 mm, respectively. Lipid content in the
hepatopancreas was of 50 to 74% with the lower values found in
animals from Nova Orleans; humidity ranged from 50 to 74%.
Concentration trends of PAH recorded in the hepatopancreas and
sediments provide, in general, (see Table 1) similar information on the
different contamination status of the mangrove areas. The prevailing
Fig. 6. ∑16 PAH/Total PAH (%) in sediments (layer 1) and hepatopancreas of Ucides cordatus from mangroves in Guanabara Bay and Guaratiba. P11 and P21: first
and second samplings in station 1 of Piedade; NO11, NO12, S11, S12: first sampling, stations 1 and 2 in Nova Orleans and Surui; NO21, NO22, S21 and S22: second
sampling station 1 and 2 in Nova Orleans and Surui; PT11 and PT12: first sampling, stations 1 and 2 in Peteca Channel; G11 and G12 first sampling, stations 1 and 2 in
Guaratiba.
Table 2
Diagnostic ratios applied to distinguish petrogenic from pyrolytic sources (Fl/P and Σ 3–6 rings PAH/Σ5 rings alkylated PAH series) and to trace oil identity (C2DBT/
C2Ph and C3DBT/C3Ph)
Shaded areas highlight values indicative of petrogenic contamination.

distribution feature of PAH homologues shown in the histogram of Fig. 7
is that of increasing concentration from C0 to Cn and, as in sediments,
hepatopancreas show, in most cases, predominance of the C2 or C3
homolog in the phenanthrene family.
Apart from Piedade, a rather uncontaminated area in Guanabara Bay,
in all other samples there is a strong predominance of phenanthrenes
(Kow: 4.57 to 6.51 for C0 to C4) which make up 30 to 46% of the Total
PAH in crabs, while in sediments phenanthrenes appeared in lesser
proportion, ranging from 6% (Guaratiba — control area) to 34% (Surui).
In animals from Nova Orleans, Surui and Peteca dibenzothiophenes,
chrysenes, pyrenes and naphthalenes are the other main components. The
high naphthalene concentrations found in Surui sediments are also
present in the hapatopancreas. Nevertheless, there is an evident dis-
criminative mechanism in the uptake and/or elimination that favors the
higher alkylated homologues. As a result, the concentration distribution
profile of the 5 alkylated PAH series in crab tissue shows closer analogy to
that of weathered oil than in the sediments. This should be expected since
bioaccumulation is influenced, among other factors, by Kows which
increase from C0 to Cn in all alkylated series.
The decrease in Total PAH from 2003 to 2004 in Surui sediments is
also recorded in the hepatopancreas (75%). This is a strong indication
of the good U. cordatus response as a biomonitor for PAH.
The diagnostic ratios (Fl/P and “Σother 3–6 rings PAH/Σ 5
alkylated PAH series”) suggest that in crabs the petrogenic imprint is
amplified in comparison to the sediments. In general, the C2DBT/C2Ph
and C3 DBT/C3 Ph ratios are not as similar to the MF380 oil ratios as
those found for sediments. Possibly, differences in bioavailability,
uptake and metabolization rates of such compounds are responsible for
the observed discrepancy. This implies that, in the application of such
tools to investigate oil source by using crabs, care has to be taken. It
should be noted that none of the studied mangroves suspected of
contamination with the MF380 oil, were originally completely free of
influences from other oil sources, since Guanabara Bay is chronically
contaminated by oil. The use of these ratios to access the presence of
certain oil in environments subjected to inputs from diverse sources is
problematic.
The Spearman test indicated strong correlation (r=0.934; pb0.05)
between PAH concentration in hepatopancreas and PAH in the top
sediment layer (0–28 cm). For the intermediate layer (28–58 cm;
r=0.789; pb0.05) correlation was weaker, but still significant. As
already mentioned, the specific crab mobility in the sediment column
contributes to push the oil front downwards. Once the contaminant is
buried, aerobic degradation becomes less likely, though the burrowing
act may eventually carry molecular oxygen deeper in the sediment.
Fig. 7. PAH distribution in hepatopancreas of Ucides cordatus from Guanabara Bay and Guaratiba mangroves. G11, G12: sampling of September 2003 at stations 1
and 2-control area-Guaratiba); P11 and P21: samplings of September 2003 and October 2004, station 1 (Piedade); NO11, NO12, PT11 and PT12: samplings of
September 2003 (Nova Orleans and Peteca); S11, S12, S21 and S22 samplings of September 2003 and October 2004 at stations 1 and 2 (Surui). PAH concentration
in μg kg− 1

This aeration, however, is evidently not sufficient to promote fast
elimination of the contaminant from the sediments. The result is that
mangrove crabs remain exposed to oil contamination for long periods
of time after a spill.
The factorial analysis of the entire data set revealed 5 factors of
which the first two are responsible for 77% of the overall variance.
Factor 1 groups mainly 4–5 rings PAH and some of the higher
alkylated homologues; factor 2 groups the majority of the 2–3 ring
alkylated and parental homologues, Ant and Ace. The 5–6 ring PAH
(ID, BghiPe), Fl are grouped in factor 4 which contributes only 6% to
the overall variance. The plot of the two major factors (Fig. 8) shows
the great majority of sediment and hepatopancreas samples in a cluster,
demonstrating that the two matrices show similar concentrations.
Outside the cluster, in the upper left part of the plot, appear the Surui
samples from station 1, layer 1, that differ from the cluster by factor 2
(concentration of compounds in factor 2), and from hepatopancreas
samples by factor 1 (higher concentration of compounds in factor 1). In
the lower part, outside the cluster, are the hepatopancreas from station 1
in Peteca, which also differ in concentration of compounds in factor 1.
The analysis underlines substantive differences in Surui samples in
relation to others, which are mainly due to higher concentrations of
light alkylated PAH.
The percentage of parental PAH in crabs is lower than in the
sediments, and varies from 11–28%, in the least contaminated areas
(Guaratiba and Piedade), to 3–10% in the other mangroves. There is an
evident dominance of alkylated PAH both in sediments and in the
hepatopancreas. Nevertheless, bioaccumulation factors (BAF was
calculated using normalization of PAH concentrations to organic
carbon content in sediments, and to lipid content in animals) for
individual compounds are variable from area to area. In Nova Orleans
and Peteca, lower molecular weight PAH show higher BAF, while in
Surui, station 1, alkylated phenanthrenes and benzo(k)fluoranthene are
favored (see Fig. 9). Preferred bioaccumulation of alkylated PAH
should be expected from the superior Kow and lipophilicity of such
compounds in relation to their parent homologues (Irwin et al., 1997),
although these same properties may render the compounds less
available for uptake from the water phase. Lamoureux and Brownawell
(1999) ascribe maximum bioaccumulation factors of hydrophobic
organic contaminants, commonly occurring at intermediate Kows
(log Kow: 6.0–6.5), to slow desorption of high Kow compounds, and
to association of low Kow compounds to resistant phases. In the present
work no correlation was found between Kows and BAF when evaluat-
ing the entire data set from a single station. However, within the series
of phenanthrenes (4.57blog Kow b6.51), fluorenes (4.18 blog
Kow b5.5), and diobenzothiophenes (4.49blog Kow b5.73) there are
good linear relations in Surui and Nova Orleans. The increase in
bioaccumulation with increasing molecular weight in these series can
be seen in Fig. 9 for Surui. The occurrence of such a relation, par-
ticularly in the most contaminated samples, can be ascribed to direct
exposure to free oil droplets in the sediments.
Melzian and Lake (1987) were possibly the first to report prevalence
of alkylated homologues of naphthalene and phenanthrene over parental
PAH in crabs exposed to No. 2 fuel oil. Hellou et al. (1994) also report
predominance of phenanthrene and alkylated phenanthrene in Chionoe-
cetes opilioand Hyas coarctatus in relation to sediments from Conception
Bay in Newfoundland. These authors found, in addition, enrichment of
benz(a)anthracene and chrysene in hepatopancreas, attributing the
concentration differences between crabs and sediments to the composi-
tion of the diet, to bioavailability and to the activity of MFO enzymatic
system. Similar to the findings of the present paper, Dugan et al. (2005)
reported that in sand crab tissues (Eremita analoga) from sandy beaches
in California, 70% or more of the Total PAH was alkylated homologues.
In the present work the observed results may be explained by: the
accumulation derived from dietary exposure as a result of direct food
contact with free oil residues found in some sediment, as for instance,
in Surui; and the variable fraction of the active organic substrate
controlling bioavailability of PAH in the different areas.
Di Toro et al. (1991) and Baumard et al. (1999) report that BAF
should preferably be used to predict bioaccumulation, since normal-
ization for organic carbon in sediments and for lipids in animals ought
to level out variability among sites and animals. Here the variability,
expressed as relative standard deviations of BAF and of accumulation
factors (AF=ratio between concentrations in sediment and hepatopan-
creas) calculated either using the Σ16 PAH or Total PAH were very
Fig. 8. Factorial analysis of PAH distribution in crabs (U. cordatus) and
sediments (all layers) from Guanabara Bay and Guaratiba. Projections have been
performed on the factorial plane (F1×F2). Factor 1 represents 57% of total
variance of the original data, and factor 2, 20%. Inset shows a zoom on the
cluster (H = hepatopancreas and S = sediment).
Fig. 9. Accumulation Factor (AF) for individual PAH; Surui mangrove, station 1, samplings (
▪) 2003 and (□) 2004 (see Fig. 2 for abbreviations).

similar, and equal to 31% and 28%, respectively. The variation of the
AF and BAF ratios for Total PAH of 0.5 to 0.05 in Piedade and 5.8 to
0.6 in Nova Orleans, showed a linear correlation characterized by the
equation AF=10.1BAF+0.58, with a correlation coefficient (r2
) of
0.941 (n=28; pb0.001). Therefore, normalization for lipid content
(62.4±6.5%) and sediment organic carbon (1.21–8.43%) did not
facilitate the observation of accumulation trends or decreased factor
variability among different sites. There was no relation between AF and
organic carbon content in sediments. These observations emphasize the
major influence of organic carbon speciation in controlling bioavail-
ability. The relatively low AF in crabs compared to those observed for
mussels (Hellou et al., 2005) may be explained because the former
present a higher level of metabolism that leads to biotransformation and
excretion of PAH as polar metabolites (Nudi, 2005).
Although chemical analysis of PAH in hepatopancreas is more
laborious than in sediments, the information obtained is of higher value
for risk assessment. Moreover, harvest of animals can be carried out
faster and requires fewer personnel in the field. This is advantageous in
mangroves where effects of oil contamination can be aggravated due to
the transit of persons. The decline in PAH concentration from 2003 to
2004 in sediments and crabs from Surui, which is credited to
heterogeneities in the sediments, is a strong indication that U. cordatus
mobility must be restricted to a rather small area. This limited drift range
is an additional advantage for the use in biomonitoring, first because
concentrations in tissues reliably represent the contamination level in a
well specified area, and secondly because the number of harvested
animals for such a purpose can be optimized, so as to reduce impact on
populations. The results of this study point out U. cordatus as an
excellent bioindicator to evaluate PAH pollution in mangrove areas.
4. Conclusions
The PAH study carried out in sediments and in hepatopan-
creas of Ucides cordatus from Guanabara Bay mangroves show
that bioaccumulation of these substances occurs in crabs from
contaminated areas such as Surui and Channel of Peteca. A
preferential accumulation of parental and alkylated PAH with
three and four rings was observed.
The determination of alkylated PAH homologues was
essential for identifying the sources of aromatic hydrocarbons
in the crabs. Except in Piedade mangrove, that is further away
from oil sources, the main source of PAH contamination in the
crabs is unequivocally petrogenic.
The crabs collected in the Surui show elevated concentrations
of oil derived PAH, which concur with observations in the
sediments. This implies an uptake of contaminants by crabs
directly from the sediments, since, given the high Kow of such
substances, concentrations in water should be too low (some tens
of ng L−1
) to explain the high content in the hepatopancreas.
Because crustaceans are capable of metabolizing PAH and
excreting the contaminants, the parity between sediment
concentration and body burden suggests continuous exposure
allied to a moderate efficiency of the MFO enzymatic system.
The statistical treatment of the entire PAH data set indicates that
the main contamination of biota occurs in the upper 28 cm of the
sediment column.
Survival in a sediment environment which contains more
than 30,000 μg kg−1
PAH proves that U. cordatus is resilient to
oil, a primary prerequisite of a good biomonitor for oil con-
tamination in mangroves. Furthermore, both the Total PAH
concentration and the individual PAH profiles found in the
hepatopancreas are reliable records of different contamination
levels in the environment and of contaminant source.
Finally, analysis of hepatopancreas proved that PAH, present
principally in the sediments, are bioavailable to the crabs. The
obtained results can also be used as a basis for evaluating risk
imposed to humans due to the common practice of ingesting
crab internal organs.
Acknowledgements
The authors are grateful to the Brazilian Research Council
(CNPq), to the Rio de Janeiro Research Foundation (FAPERJ)
and to the Brazilian Coordination for Capacity Building
(CAPES) for financial support. The collaboration of Dr. Renato
Carreira is acknowledged.
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