Gc PAH Oil Refinary

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Petroleum contamination impact on macrobenthic communitiesunder the influence of an oil refinery: Integrating

chemical and biological multivariate data

Natalia Venturini a,*, Pablo Muniz b, Marcia C. Bıcego a, Cesar C. Martins a,d,Luiz Roberto Tommasi c

a Instituto Oceanogr afico da Universidade de S~ao Paulo (IOUSP), Praca do Oceanografico 191, Cidade Universitari a, 05508-900 S~ao Paulo, SP, Brazil b Seccion Ocean ologı a, Departamento de Ecologıa, Facultad de Ciencias, Igua 4225, 11400 Montevideo, Uruguay

c Fundac~ao de Estudos e Pesquisas Aquaticas (FUNDESPA), Av. Afrani o Peixoto 412, 05507-000 S~ao Paulo, SP, Brazil d Centro de Estudos do Mar da Universidade Federal do Parana (UFPR), Caixa Postal 50.002, Pontal do Sul, 83255-000, Pontal do Parana, PR, Brazil

Received 1 February 2006; accepted 18 January 2008

Available online 1 February 2008

Abstract

Petroleum contamination impact on macrobenthic communities in the northeast portion of Todos os Santos Bay was assessed combining in

multivariate analyses, chemical parameters such as aliphatic and polycyclic aromatic hydrocarbon indices and concentration ratios with benthic

ecological parameters. Sediment samples were taken in August 2000 with a 0.05 m2 van Veen grab at 28 sampling locations. The predominance

of n-alkanes with more than 24 carbons, together with CPI values close to one, and the fact that most of the stations showed UCM/resolved

aliphatic hydrocarbons ratios (UCM:R) higher than two, indicated a high degree of anthropogenic contribution, the presence of terrestrial plant

detritus, petroleum products and evidence of chronic oil pollution. The indices used to determine the origin of PAH indicated the occurrence of

a petrogenic contribution. A pyrolytic contribution constituted mainly by fossil fuel combustion derived PAH was also observed. The results of the stepwise multiple regression analysis performed with chemical data and benthic ecological descriptors demonstrated that not only total PAH

concentrations but also specific concentration ratios or indices such as !C24:<C24, An/178 and Fl/Fl þ Py, are determining the structure of

benthic communities within the study area. According to the BIO-ENV results petroleum related variables seemed to have a main influence

on macrofauna community structure. The PCA ordination performed with the chemical data resulted in the formation of three groups of stations.

The decrease in macrofauna density, number of species and diversity from groups III to I seemed to be related to the occurrence of high aliphatic

hydrocarbon and PAH concentrations associated with fine sediments. Our results showed that macrobenthic communities in the northeast portion

of Todos os Santos Bay are subjected to the impact of chronic oil pollution as was reflected by the reduction in the number of species and di-

versity. These results emphasise the importance to combine in multivariate approaches not only total hydrocarbon concentrations but also in-

dices, isomer pair ratios and specific compound concentrations with biological data to improve the assessment of anthropogenic impact on

marine ecosystems.

Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: oil refinery; sediments; hydrocarbon ratios; macrofauna; ecological descriptors; multivariate analyses

1. Introduction

Coastalareas are directly subjected to anthropogenic impacts

mainly derived from industrial and urban activities. Although

hydrocarbons presence in the marine environment can originate

from natural sources such as forest fires, natural petroleum seeps

and post-depositional transformations of biogenic precursors,

a large proportion can be attributed to human activities. Urban

runoff, sewage disposal, industrial effluents, oil production

and transportation are some of the most important sources of an-

thropogenic hydrocarbons (Kim et al., 1999).* Corresponding author.

E-mail address: [email protected] (N. Venturini).

0272-7714/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2008.01.008

Available online at www.sciencedirect.com

Estuarine, Coastal and Shelf Science 78 (2008) 457e467www.elsevier.com/locate/ecss

mailto:[email protected]

http://www.elsevier.com/locate/ecss

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mailto:[email protected]





fractionated by silicaealumina gel chromatography into ali-

phatic and aromatic hydrocarbons.

Aliphatic fractions were determined by injecting 2 ml of the

concentrated extracts into a HP 5890A Series II gas chromato-

graph (GC) with a flame ionisation detector (FID). Aromatic

fractions were determined by injecting 1 ml of the concen-

trated extracts on a Fisons Trio 1000 GC, with a mass spec-

trometry (MS) detector, and detection operated under the

SIM (selected ion monitoring) mode. The instrument detection

limit was based on the lowest concentration of a calibration

standard mixture and it was 0.01 ng gÀ1 for CG-MS and

0.10 ng gÀ1 for CG-FID. The capillary column used was

a HP Ultra II (25 m long, 0.32 mm i.d., 0.25 mm film thick-

ness) programmed from 40e60 C at 20 C minÀ1, 60e

300 C at 4 C minÀ1 and held at 300 C for 10 min. The an-

alytical program was conducted under controlled laboratory

conditions, following a laboratory quality assurance protocol.

In order to evaluate the accuracy and the precision of the anal-

ysis two replicates of the National Institute of Standards

(NIST) standard reference sediment SRM 1941a (Organics

in Marine Sediment) were analysed. The average concentra-

tions agreed with the certified concentrations for all com-

pounds analysed. The relative standard deviation (RSD) of

the replicates ranged from 0.3% to 12.8%. For aliphatic hydro-

carbons, regular analyses of reference material from the Interna-

tional Atomic Energy Agency (IAEA-383) gave satisfactory

results. The average concentrations agreed with the available

certified concentrations for selected compounds (n-C17, n-C18,

pristine, phytane), total n-alkanes and resolved aliphatics.

The RSD of the two replicates ranged from 9.4% to 24.6%.

Detection limits (DL) in sediments ranged between 0.31 and

1.23 ng gÀ1 dry weight for PAH analytes and between 0.10

and 7.41 ng gÀ1 for n-alkanes and isoprenoids. They were cal-

culated as three times the mean concentration of method

blanks for each PAH (Citac/Eurachem Guide, 2002).

Since natural samples consist of complex hydrocarbon mix-

tures, several parameters in addition to absolute concentrations

were used as distinct tracers to identify possible sources of al-

iphatic and aromatic hydrocarbons in sediments.

Faunal samples were also taken using a 0.05 m2 van Veen

grab. Three replicate (pooled) samples were taken at each sta-

tion; the material was sieved on a 0.5 mm mesh and preserved

in 4% buffered formaldehyde. Benthic organisms from sedi-

ments were sorted, identified to the lowest possible taxonomic

level and counted. Most taxa were identified to the species

level.

12°42'

12°45'

BRAZILBAHIA

PACIFICOCEAN

ATLANTICOCEAN

5

12

34

109

87

6

1112

1314

15

2221

2019

1817

16

2324

2526

27

28

MADRE DEDEUSISLAND

MARÉISLAND

38°36' 38°32'

N

S

W E

ETDIS

MATARIPERIVER

CAIPE RIVER SÃO PAULO

1 km

RLAM

TEMADRE

TODOS OS

SANTOS BA Y

Salvador

I t a p a

r i c a I

s l a n d

ATLANTIC OCEAN

RIVER

Fig. 1. Map of the northeast portion of Todos os Santos Bay, showing the 28 sampling locations. RLAM, oil refinery; S, water-oil separator; ETDI, effluent treat-ment station; TEMADRE, marine terminal.

459 N. Venturini et al. / Estuarine, Coastal and Shelf Science 78 (2008) 457 e 467



A correlation-based PCA ordination was performed using

the computer software PRIMER (Clarke and Warwick,

1994) to identify any meaningful pattern from the samples

in relation to the percentage of fine sediments (silt þ clay), to-

tal hydrocarbon concentrations and chemical parameters. To

avoid the problem of comparing variables with different units,

and therefore, with different scales of variation, data were pre-viously standardised ( x i À m / s) (Zar, 1996). Density was esti-

mated as the total number of individuals ( N ) per unit area

(0.15 m2) and species richness as the total number of species

(S ). Diversity ( H 0, loge) was estimated by the Shannone

Wiener index (Shannon and Weaver, 1963) and evenness ( J 0)

according to Pielou (1966). In order to determine which of

the chemical parameters used explained best the variation in

community descriptors (S, density and H 0), a stepwise multiple

regression analysis was applied using the computer pro-

gramme STATISTICAÒ (StatSoft Inc, 1995). This analysis

compares the relative importance of the independent variables

(chemical ones) in explaining the variance of the dependent

variables (biological ones); through the construction of a multi-linear model (Zar, 1996). The relationship between multivari-

ate environmental data and biological data (species abundance

matrix) was achieved applying the BIO-ENV procedure

(Clarke and Ainsworth, 1993). The best matches of abiotic

and biotic (dis)similarity matrices were measured using the

weighted Spearman rank correlation coefficient (rw). Macrofauna

species abundance data were previously four-root transformed

and the BrayeCurtis similarity measurements used for the con-

struction of the biotic matrix. A one-way analysis of similarities

(ANOSIM) was performed to test the differences in macro-benthic species abundance among the groups of stations obtained

in the PCA (Clarke and Green, 1988). To establish which species

contributed the most to differences observed among groups, the

similarity percentages analysis (SIMPER) was applied.

4. Results

4.1. Aliphatic and aromatic hydrocarbons

Mean concentration of total aliphatic hydrocarbons within

the study area was 34.90 mg gÀ1 dry weight. Lowest concen-

trations were recorded at stations 1 and 2 (1.56 and

1.76 mg gÀ1, respectively) and highest values at stations 9and 12 (236.42 and 246.91 mg gÀ1, respectively) (Table 1). To-

tal n-alkanes varied from 0.86 to 39.94 mg gÀ1 with a predom-

inance of n-alkanes with more than 24 carbons as indicated by

Table 1

Percentage of fine sediments (<0.63 mm), concentrations and values of the evaluation indices applied to aliphatic and aromatic hydrocarbons detected in sediment

samples of Todos os Santos Bay. Aliph, total aliphatic hydrocarbons; n-alk, total n-alkanes; UCM, unresolved complex mixture; R, resolved aliphatics; UCM:R,

unresolved complex mixture/resolved aliphatic hydrocarbons ratio; alkanes !3n-C24:<n-C24 ratio; CPI, carbon preference index based on Commendatore et al.

(2000); PAH, total polycyclic aromatic hydrocarbons; An/178, anthracene/anthracene þ phenantrene ratio; Fl/Fl þ Py, fluoranthene/fluorantheneþ pyrene ratio;

IP/IP þ BghiP, indeno [1,2,3-c,d ] pyrene/indeno [1,2,3-c,d ] pyrene þ benzo [g,h,i] perylene; LMW, PAH with two to three aromatic rings; HMW, PAH with

four to six aromatic rings; n.d., not detected; e, not calculated

St. Silt þ clay(%)

Aliph(mg gÀ1)

n-alk (mg gÀ1)

UCM(mg gÀ1)

R(mg gÀ1)

UCM:R !C24:<C24 CPI PAH(ng gÀ1)

An/178 Fl/FlþPy IP/IPþBghiP LMW/HMW

1 0.10 1.76 0.86 n.d. 1.76 e 1.25 1.03 310.00 e 0.50 0.62 13.34

2 4.20 1.56 1.15 n.d. 1.56 e 0.75 1.17 304.50 e 0.49 0.34 4.72

3 0.20 48.14 2.74 40.05 8.09 4.95 0.50 0.91 18.30 e 0.23 0.46 1.14

4 9.10 43.89 6.42 35.72 8.16 4.38 1.59 0.76 107.50 0.16 0.23 0.25 0.22

5 91.60 199.36 14.12 119.70 79.66 1.50 1.46 0.62 4163.00 0.80 0.22 0.75 0.47

6 92.40 112.74 8.04 93.68 19.06 4.92 2.56 1.60 283.40 0.22 0.48 0.39 0.13

7 22.30 56.34 6.35 40.32 16.02 2.52 1.09 2.01 94.86 0.35 0.33 0.23 0.55

8 89.60 75.82 2.46 50.96 24.86 2.05 1.76 1.54 1355.00 0.84 0.54 0.74 0.22

9 91.20 236.42 6.82 131.67 104.75 1.26 1.67 1.80 293.40 0.64 0.43 0.39 0.28

10 0.20 25.96 1.73 22.97 2.98 7.71 1.07 e 11.56 e 0.36 0.40 0.10

11 93.20 41.95 1.57 36.96 4.98 7.42 1.21 1.70 38.56 e e 0.38 0.25

12 91.70 246.91 5.83 189.01 57.89 3.26 1.21 0.63 727.10 0.67 0.50 0.87 0.39

13 95.70 37.99 5.33 18.31 19.68 0.93 3.01 0.91 779.90 0.65 0.46 0.89 0.37

14 94.60 112.79 5.93 55.22 57.56 0.96 1.80 1.26 1614.00 0.72 0.09 0.86 0.20

15 0.10 70.15 8.65 67.67 2.48 27.29 1.40 0.77 547.10 0.02 0.44 0.95 15.57

16 89.60 163.15 8.15 143.84 19.32 7.45 12.48 3.22 888.10 0.04 0.51 0.92 0.09

17 0.20 38.77 5.22 33.52 5.25 6.38 2.66 1.06 32.29 e 0.20 0.72 0.21

18 93.60 68.46 7.93 49.09 19.37 2.53 1.17 0.89 2969.00 0.21 0.58 0.82 0.54

19 98.40 39.25 5.47 26.95 12.30 2.19 1.13 0.65 403.50 0.29 0.64 0.38 0.16

20 96.60 43.32 6.05 29.30 14.02 2.09 1.23 1.41 381.50 0.48 0.49 0.48 0.23

21 93.00 50.17 9.63 31.61 18.56 1.70 0.60 0.60 523.80 0.48 0.44 0.38 0.27

22 0.10 5.15 3.16 n.d. 5.15 e 1.05 e 149.30 e 0.68 0.90 0.13

23 10.80 24.01 1.14 21.43 2.58 8.31 0.25 e 22.51 e 0.55 0.26 0.08

24 0.10 2.93 1.38 n.d. 2.93 e 0.11 e 8.29 e 0.54 e 0.29

25 92.50 23.78 15.17 6.27 17.51 0.36 11.42 0.19 1043.00 0.08 0.64 0.38 0.32

26 79.40 113.88 39.94 57.09 56.79 1.01 8.37 2.65 773.40 0.43 0.44 0.91 0.13

27 85.20 75.97 3.78 63.24 12.73 4.97 5.99 1.93 1470.00 0.08 0.39 0.44 0.17

28 9.50 34.90 1.93 25.56 9.34 2.74 1.41 3.21 685.90 0.05 0.44 0.85 1.38




the !C24:<C24 ratio. These high molecular weight n-alkanes

showed high concentrations at stations 16, 25, 26 and 27,

which are located near the mouth of the S~ao Paulo River (Ta-

ble 1). Resolved aliphatic concentrations varied between 1.56

(station 2) and 104.75 mg gÀ1 (station 9). The unresolved com-

plex mixture (UCM) varied from non-detected at stations 1

and 2 to 189.01 mg gÀ1

at station 12 (Table 1). At the majorityof the stations the UCM represented between 60 and 96% of

the total aliphatic hydrocarbons. In addition, most of the sta-

tions showed UCM/resolved aliphatic hydrocarbons ratios

(UCM:R) higher than two and carbon preference index

(CPI) values close to one (Table 1). In general, the stations sit-

uated in the centre and in the east region of the study area

showed higher aliphatic hydrocarbons than the others (Fig. 2).

The 23 PAH compounds detected in sediment samples were

naphthalene, 1- and 2-methylnaphthalene, biphenyl, 2,6-dime-

thylnaphthalene, 2,3,5-trimethylnaphthalene, acenaphthylene,

acenaphthene, fluorene, phenanthrene, anthracene, 1-methyl-

anthracene, fluoranthene, pyrene, chrysene, benzo[b]- and

benzo[k ]fluoranthene, benzo[e]- and benzo[a]pyrene, pery-lene, dibenzo[a,h]anthracene, indeno[1,2,3-c,d ]pyrene and

benzo[g,h,i]perylene.

Total PAH concentrations were expressed as the sum of the

23 compounds listed above; being that the mean concentration

for the whole area was 899.58 ng gÀ1. The lowest value was

recorded at station 24 (8.29 ng gÀ1) and the highest at station

5 (4163 ng gÀ1), which is located adjacent to the effluent’s

treatment station of the oil refinery (Table 1). Spatially, PAH

concentrations were higher at the stations situated in the centre

and in the east region of the study area than in the others

(Fig. 2). The anthracene/anthracene þ phenantrene ratio (An/ 178) varied between 0.02 and 0.84, and only stations 15, 16,

25, 27 and 28 showed values <0.10 (Table 1). Stations 3, 4,

5, 7, 10, 14, 17 and 27 showed fluoranthene/fluoranthene þpyrene ratios (Fl/Fl þ Py) <0.40, whereas the others showed

values between 0.40e0.50 or >0.50 (Table 1). Values of

the indeno[1,2,3-c,d ]pyrene/ indeno[1,2,3-c,d ]pyrene þ benzo

[g,h,i]perylene ratio (IP/IP þ BghiP) were >0.50 at stations

situated in the centre and in the east region of the study

area. The others showed values between 0.20 and 0.50 (Table

1). Based on Yunker et al. (2002), the isomer pair ratios An/

178 and IP/IPþ BghiP were plotted against Fl/Fl þ Py to

show how PAH distribute in relation to their possible sources.

According to these ratios most of the samples are influencedprimarily by petroleum and petroleum combustion sources

(Fig. 3). The ratio between the volatile PAH with two to three

aromatic rings and the high molecular weight PAH with four

to six aromatic rings (LMW/HMW) was <1 at all of the sta-

tions except 1, 2, 3, 15, and 28 (Table 1).

4.2. Community analysis

A total of 543 individuals were recorded that belong to 55

macrobenthic species. Polychaeta was the most abundant

12

34 5

67

89

10

1112

1314

15

16

1718

1920

212223

2425

2627

28

RLAM

SETDI

Total PAH

1 2

34

5

67

89

10

1112

1314

15

16

1718

1920

2122

2324

2526

27

28

RLAM

S

ETDI

Total Aliphatic

Hydrocarbons

Fig. 2. Maps showing the spatial distribution of total aliphatic hydrocarbons

(mg gÀ1 dry weight) and total polycyclic aromatic hydrocarbons (PAH)

(ng gÀ

1 dry weight) in the northeast portion of Todos os Santos Bay.

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8

A n / 1 7 8

0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1

0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8

Fl/Fl + Py

I P / I P

+ B g h i P

PetroleumPetroleum

Combustion

Grass/wood/coal

Combustion

Petroleum

Petroleum

Grass/wood/coal

Combustion

Petroleum

Combustion

Combustion

A

B

Fig. 3. Plots for the PAH isomer pair ratios of the 28 sediment samples of To-

dos os Santos Bay based on Yunker et al. (2002): (A) An/178 versus Fl/

Fl þ Py and B) IP/IP þ BghiP versus Fl/Fl þ Py.




group with 73.84% of the individuals, following by Mollusca

and Crustacea with 14.54% and 9.57%, respectively. Species

richness according to the total number of species rangedfrom 0 at station 5 to 13 at station 22 (Table 2). The highest

density values (ind. 0.15 mÀ2) were recorded at stations 1, 3,

4, 10, 15, 17, 22, 23 and 28. At station 3 the high density

was exclusively by the presence in great abundance of the

polychaete Ophelina sp. Diversity ranged from 0.21 at station

3 to 2.39 at station 17 and evenness varied between 0.31 to 1

(Table 2). In general, low diversity values corresponded to the

stations situated in the centre and in the east region of the

study area. Evenness lowest values corresponded to stations

1, 3 and 4 and they were related to the dominance of the poly-

chaete Ophelina sp. in the former stations and Goniada littorea

in the latter.

4.3. Hydrocarbons and macrofauna, multivariate

analyses

The results of the stepwise multiple regression analysis are

shown in Table 3. When the number of species (S ) was con-

sidered as the dependent variable, significant partial correla-

tion coefficients ( p < 0.05) were obtained with total PAH

concentrations, the !C24:<C24, An/178 and Fl/Fl þ Py ra-

tios. The multiple correlation coefficient ( R) was 0.73 and

the multiple determination coefficient ( R2) was 0.53. Consid-

ering the density of macrobenthic organisms as the dependent

variable, a significant partial correlation coefficient ( p < 0.05)

was obtained with the percentage of fine sediments (silt þ

clay). In this case, the multiple correlation coefficient and

the multiple determination coefficient were R ¼ 0.49 and

R2¼ 0.24, respectively. Furthermore, a significant partial cor-

relation coefficient between diversity ( H 0) and total PAH con-

centrations was also obtained, with R ¼ 0.49 and R2¼ 0.25.

The PCA ordination performed with the chemical data and

the percentage of muddy sediments resulted in the formation

of three groups of stations (Fig. 4). The first component

(PC1) explained 37.3% of the variance and the second compo-

nent (PC2) 14.9%. The first axis showed negative correlation

with the percentage of fine sediments (siltþ

clay), aliphatichydrocarbons, n-alkanes, UCM, the An/178 ratio and PAH

concentrations, whereas, the second axis showed positive cor-

relation with the UCM/resolved aliphatic ratio and negative

correlation with the Fl/Fl þ Py ratio (Table 4). In general,

stations of groups I and II presented higher aliphatic, UCM

Table 2

Total number of species (S ), density (ind. 0.15 mÀ2), diversity ( H 0 loge) and

Pielou’s evenness ( J 0) of the 28 samples of Todos os Santos Bay

St. S Density H 0 J 0

1 4 25 0.92 0.66

2 1 4 e e

3 2 201 0.21 0.31

4 3 15 0.63 0.575 0 0 e e

6 6 10 1.61 0.90

7 6 7 1.75 0.98

8 1 1 e e

9 7 11 1.85 0.95

10 12 27 2.27 0.91

11 5 10 1.50 0.94

12 2 4 0.56 0.81

13 3 4 1.04 0.95

14 2 3 0.64 0.92

15 8 34 1.40 0.67

16 3 4 1.04 0.95

17 13 27 2.39 0.93

18 3 4 1.04 0.95

19 4 6 1.33 0.96

20 6 8 1.73 0.97

21 5 8 1.56 0.97

22 13 40 2.20 0.86

23 10 22 1.92 0.83

24 4 8 1.32 0.95

25 2 3 0.64 0.92

26 2 2 0.69 1.00

27 3 7 0.96 0.87

28 8 44 1.68 0.81

Table 3

Results of the stepwise multiple regression analysis. Significant partial corre-

lation coefficients ( p < 0.05) (b) are in bold. b, partial correlation coefficient;

R, multiple correlation coefficient; R2, multiple determination coefficient

Independent variables

that entered the modelab R R2

Dependent variable: S (number of species)

PAH L0.39 0.73 0.53UCM:R 0.26

! C24:<C24 L0.38

An/178 L0.42

Fl/Fl D Py L0.39

IP/IP ¼ BghiP 0.38

Dependent variable: D (density)

Silt D clay L0.44 0.49 0.24

Fl/Fl þ Py À0.18

Dependent variable H 0 (diversity)

PAH L0.49 0.49 0.25

a Abbreviations are the same as in Table 1.

PC1 (37.3 %)

P C 2 ( 1 4 . 9

% )

5

269

14

16

12

2120

19

25

1318

8

27

67

28

1117

4

3

10

23

21

2224

I

II

III

+ -

Silt+clay, aliphatics, n-alkanes, UCM, An/178, PAH

+

-

U C M : R e s o l v e d a l i p h a t i c s

15

F l / F l + P y

+

-

Fig. 4. PCA ordination diagram of the 28 sampling stations of Todos os Santos

Bay based on chemical data and the percentage of muddy sediments.




and PAH mean concentrations than the stations of group III

(Table 5).

ANOSIM results (Global R ¼ 0.267, significance level

(sl) ¼ 0.1%; pairwise tests: RI,III ¼ 0.449, sl¼ 0.3%;

RI,II ¼ 0.168, sl ¼ 4.5%; RII,III ¼ 0.197, sl ¼ 0.9%) showed

the three groups of stations obtained in the PCA differing sig-

nificantly in relation to their macrobenthic species abundance.

The difference was high between groups I and III, but not for

group II. In fact, group II showed mean species number and

density values similar to those recorded at group I, and

mean diversity similar to group III (Table 5). According to

the SIMPER results the dissimilarity among the three groups

was high. In group I the number of species and their relative

abundance was lower than in group II and III (Table 6). The

species that contributed the most to the dissimilarity between

group I and III were Sigambra grubii and Dasybranchus cf.

platyceps that occurred only in group I, Goniada littorea and

Nematonereis schmardae that were absent in group I and

Table 4

Results of the principal component analysis (PCA) performed with chemical

data of the 28 sediment samples of Todos os Santos Bay

Eigenvalues %Variation Cum. % Variation

PC1 3.73 37.3 37.3

PC2 1.49 14.9 52.2

Eigenvectors

Variablea PC1 PC2

Silt þ clay À0.392 À0.288

Aliph À0.454 0.172

n-alk À0.261 À0.045

UCM À0.415 0.292

CPI À0.217 0.25

UCM:R 0.059 0.664

PAH À0.336 À0.197

An/178 À0.395 À0.276

Fl/Fl þ Py 0.06 À0.357

IP/IP ¼ BghiP À0.277 0.232

a Abbreviations are the same as in Table 1.

Table 5

Means of the biological and chemical parameters in each of the three groups

obtained in the PCA ordination. Abbreviations are the same as in Table 1

Group I Group II Group III

S 3 4 7

Density (ind. 0.15 mÀ2) 4 6 36

H 0 0.80 1.10 1.40

J 0 0.77 0.83 0.72

Silt þ clay (%) 89.68 93.00 11.55

Aliph (mg gÀ1) 178.67 58.61 30.42

n-alk (mg gÀ1) 13.46 7.09 3.25

UCM (mg gÀ1) 116.08 41.04 24.93

R (mg gÀ1) 62.66 12.73 9.34

UCM:R 2.57 2.42 7.97

! C24:<C24 4.50 3.21 1.10

CPI 1.70 1.08 1.40

PAH (ng gÀ1) 1409.83 1023.23 303.23

An/178 0.55 0.37 0.15

Fl/Fl þ Py 0.37 0.52 0.41

IP/IP þ BghiP 0.78 0.55 0.53

LMW/HMW 0.26 0.27 2.92

Table 6

Relative abundances of macrobenthic species in the three groups of stations

and average dissimilarities among them according to SIMPER results. Species

which contributed most to differences among the groups are in bold. Average

dissimilarity between Groups I & II ¼ 94.46. Average dissimilarity between

Groups I & III ¼ 96.93. Average dissimilarity between Groups II &

III ¼ 90.42Species Relative abundance (%)

Group I Group II Group III

Pseudeurythoe ambigua e e 0.43

Sigambra grubii 19.23 e e

Autolytus sp. e e 3.00

Laeonereis culveri e 3.92 0.21

Goniada littorea e 3.92 9.01

Goniadides uncata e e 2.15

Glycinde multidens e 19.61 2.58

Mooreonuphis nebulosa 7.69 e 0.21

Eunice guanica e e 0.43

Eunice (N.) imogena 7.69 e 0.43

Eunice rubra e e 0.21

Nematonereis schmardae e 1.96 7.73 Lumbrineris cf. tetraura 7.69 e 0.64

Scoloplos (L.) dubia e e 0.64

Scoloplos treadwelli 3.85 e e

Cirrophorus branchiatus e 7.84 1.07

Magelona variolamelata e 1.96 0.43

Poecilochaetus sp. e 1.96 e

Audouinia sp. e 1.96 0.21

Armandia agilis e e 1.07

Ophelina sp. e 1.96 44.42

Sternaspis sp. e e 2.79

Dasybranchus cf. platyceps 11.54 1.96 e

Periclimenes americanus e 1.96 e

Alpheus sp. 7.70 7.84 e

Ogyrides alphaerostris e 1.96 e

Processa bermudensis e e 0.43 Processa hemphilli e e 0.21

Trachypenaeus constrictus e e 0.21

Paguristes sp. e e 0.64

Panopeus lacustris e e 0.21

Cyrtoplax spinidentata 3.85 e e

Pinnixa sayana e e 0.64

Leptochelia sp. e 1.96 1.72

Cyathura sp. e 1.96 0.64

Amakusanthura sp. e 1.96 2.15

Leucothoe spinicarpa e 3.92 0.43

Heterophoxus videns e e 0.86

Ischnochiton sp. e e 0.43

Neritina virginea e e 1.72

Olivella floralia e e 0.64

Nucula semiornata 3.85 3.92 0.43 Plicatula gibbosa e e 0.86

Ctena pectinella e e 1.07

Diplodonta punctata 3.85 3.92 0.21

Trachycardium muricatum e e 0.64

Tellina versicolor 7.69 7.84 0.86

Tagelus plebeius e e 1.07

Chione cancellata 11.54 e 0.86

Anomalocardia brasiliana 3.85 1.96 1.07

Callista maculata e e 0.21

Corbula caribaea e 13.73 1.72

Thysanocardia sp. e e 0.43

Lytechinus variegatus e e 0.21

Branchiostoma platae e e 1.72




Ophelina sp., which occurred only in group III (Table 6). In

addition, the polychaetes Goniada littorea, Glycinde multi-

dens, Nematonereis schmardae, Ophelina sp., and the bivalve

Corbula caribaea were the species with highest contribution to

the difference between groups II and III. These species were

recorded in both groups of stations; nevertheless, their relative

abundance varied from one group to the other (Table 6). More-over, Sigambra grubii and Chione cancellata were present in

group I with a high relative abundance but were absent in

group II, whereas with Glycinde multidens and Corbula cari-

baea the opposite was observed. These were the species that

contributed the most to the dissimilarity between these two

groups of stations.

The results of the BIO-ENV procedure showed that silt þ

clay, n-alkanes, PAH, An/178 and IP/IP þ BghiP (rW¼ 0.424)

was the combination of variables that bestmatched the biological

data, but other combinations, which included only petroleum re-

lated variables showed similar values (Table 7).

5. Discussion

5.1. Hydrocarbons

Concentrations of total aliphatic hydrocarbons in unpol-

luted intertidal and estuarine sediments are normally lower

than 10 mg gÀ1 (UNEP, 1991). In addition, total aliphatic hy-

drocarbon concentrations may reach values up to 100 mg gÀ1

in organically enriched sediments with a significant n-alkanes

source derived from higher plants (Volkman et al., 1992).

However, values higher than this, such as those recorded at

stations 5, 6, 9, 12, 14, 16 and 26 in the northeast portion of

Todos os Santos Bay, are indicative of petroleum inputs (Volk-man et al., 1992). Furthermore, total aliphatic hydrocarbon

concentrations detected in this study are similar to those re-

corded in other highly contaminated areas on the Atlantic

coast of South America (e.g. Nishigima et al., 2001; Muniz

et al., 2004). In general, petroleum shows no predominance

of odd or even carbon chains, although, long chain n-alkanes

inputs from terrestrial plant can often obscure the petroleum

derived signal (Volkman et al., 1992). In the present study,

the predominance of n-alkanes with more than 24 carbons, to-

gether with CPI values close to one suggest the presence of

both terrestrial plant material and petroleum products. Similar

results were reported by Guerra-Garcıa et al. (2003). The

occurrence of the unresolved complex mixture (UCM) and

its magnitude are considered to be related to the presence of

degraded oil and the degree of anthropogenic contribution

(Commendatore et al., 2000). In most of the stations of the

northeast portion of Todos os Santos Bay, the UCM repre-

sented between 60% and 96% of the total aliphatic hydrocar-

bons, and the UCM/resolved aliphatic hydrocarbons ratios(UCM:R) were higher than two, indicating a high degree of

anthropogenic contribution and the presence of petroleum de-

graded residues. In addition, high values of the UCM, such as

those recorded in the present study, have been previously re-

ported as evidence of chronic oil-pollution (Gogou et al.,

2000).

Total PAH concentrations in surface sediments were similar

to those recorded in other coastal areas that receive large an-

thropogenic inputs derived from urban and industrial activities

(Kim et al., 1999; Soclo et al., 2000; Muniz et al., 2005 ).

Highest values were recorded at the stations located in the cen-

tre and in the east region of the study area associated with

muddy sediments. Since PAH are hydrophobic, they tend tobe adsorbed or encapsulated by organic particles and to accu-

mulate in fine sediments (Law and Biscaya, 1994; Yunker

et al., 2002). Furthermore, among other organic particles, ter-

restrial plant detritus in the study area could act as both sour-

ces and favourable adsorption matrices of PAH in the

sediments (Wang et al., 2001). According to Notar et al.

(2001) total PAH concentrations higher than 500 ng gÀ1 are

indicative of relatively highly contaminated samples, and our

data showed that at station 5 and at the stations situated in

the centre and in the east region of Todos os Santos Bay this

value was exceeded.

PAH of molecular mass 178 and 202 (An/178 and Fl/ Fl þ Py ratios) are often used to distinguish between petro-

leum and combustion sources (Soclo et al., 2000). These iso-

mer pair ratios showed that PAH in sediments of Todos os

Santos Bay derive from both kinds of sources. Most of the sta-

tions showed An/178 ratios >0.10 indicating the dominance of

combustion sources (Oros and Ross, 2004). Besides, stations

3, 4, 5, 7, 10, 14, 17 and 27 showed Fl/Fl þ Py < 0.40,

whereas other stations showed values between 0.40 and

0.50, suggesting the dominance of petroleum (crude oil) and

petroleum combustion sources, respectively. In areas located

close to crude oil refineries, it is expected to find an important

contribution of PAH produced by the refining process, which

can enter the marine environment through air emissions and

wastewater effluents (Oros and Ross, 2004). Furthermore,

some of the stations presented Fl/Fl þ Py ratios >0.50, which

according to Yunker et al. (2002) are values characteristic of

grass, wood or coal combustion Regarding the IP/IP þ BghiP

ratios, half of the stations showed the dominance of liquid fos-

sil fuel (e.g. vehicles and crude oil) combustion sources with

values between 0.20 and 0.50. The other half presented the

dominance of PAH derived from the combustion of coal,

grasses and wood. In general, these ratios showed that in sed-

iment samples of Todos os Santos Bay PAH are derived from

both, direct inputs of petroleum and combustion sources. In

addition, LMW/HMW ratios <1 indicated the predominance

Table 7

Summary of the BIO-ENV results for the Todos os Santos Bay data. Only the

best correlation are shown. Overall optimum weighted Spearman rank corre-

lation coefficient (rw) is in bold. Abbreviations are the same as in Table 1

No. of variables Best variable combinations (rw)

1 PAH (0.327)

2 n-alk, PAH (0.413)

3 n-alk, PAH, An/178 (0.406)

4 n-alk, PAH, An/178, IP/IP þ BghiP (0.421)

5 Silt D clay, n-alk, PAH, An/178,

IP/IP D BghiP (0.424)

6 Siltþclay, Aliph, n-alk, PAH,

An/178, IP/IP þ BghiP (0.408)




of four to six aromatic ring or soot PAH derived from high-

temperature combustion processes (Oros and Ross, 2004).

The predominance of HMW PAH may be related to the

slow degradation and high persistence of these compounds

in marine sediments (Readman et al., 2002). Overall, the indi-

ces used to determine the origin of PAH indicated the occur-

rence of a petrogenic contribution (i.e. unburned petroleum)and a pyrolytic contribution constituted mainly by PAH de-

rived from fossil fuel (petroleum) combustion in sediment

samples of Todos os Santos Bay.

5.2. Macrofauna and hydrocarbons relationships

In general, the factors that determined the structure of ben-

thic communities can be classified as abiotic (e.g. sedimentary

characteristics, salinity, depth), biotic (e.g. food availability,

interactions among species) and anthropogenic (e.g. derived

from urban and industrial activities). They are inter-related

and have synergic effects.

The BIO-ENV procedure established that the combinationof variables that best matched to the biological data was

silt þ clay, n-alkanes, PAH, An/178 and IP/IPþ BghiP, al-

though other combinations which included only petroleum re-

lated variables showed similar Spearman rank correlation

values. Some studies have proposed that the distribution and

partitioning of nonpolar organic contaminants, such as PAH

to marine sediments is controlled by the amount of organic

carbon, soot carbon, humic acid content, polarity and surface

area of sediment particles (Burgess et al., 2001 and references

therein). Certainly, hydrocarbon concentrations are influenced

by sedimentary characteristics such as grain size and organic

carbon content of the sediments, which in turn influence distri-butional patterns of macrofauna. However, the present study

showed that hydrocarbon concentrations have a relevant influ-

ence on macrobenthic communities, and this was evident

through the relationships between the abiotic indices and ra-

tios employed and the biological patterns observed.

Furthermore, the results of the stepwise multiple regression

analysis performed with chemical data and benthic ecological

descriptors demonstrated that, granulometry (content of

muddy sediments) or total PAH concentrations are not the

only parameters determining the structure of benthic commu-

nities. Besides, the number of species and diversity showed

a relationship with specific concentration ratios or indices

such as !C24:<C24, An/178 and Fl/Fl þ Py. As stated before,

terrestrial plant detritus could act as both source and favour-

able adsorption matrices of PAH (Wang et al., 2001). Detritus

derived from terrestrial plants are present in the study area and

they constitute a relatively more recalcitrant fraction of or-

ganic matter, which tends to accumulate and be more persis-

tent in the sediments. Several studies have demonstrated that

the organic enrichment of marine sediments can result in

a gradual diminishing of macrofauna abundance, species rich-

ness, and also in a significant reduction of diversity in highly

perturbed environments (Pearson and Rosenberg, 1978; Nils-

son and Rosenberg, 1994; Jewett et al., 1999; Frouin, 2000

among others). Therefore, the negative partial correlation

obtained between the !C24:<C24 index and the number of

species was not surprising.

Some characteristics make PAH potentially harmful sub-

stances. They have high solubility in lipids, some of them

have carcinogenic and mutagenic effects and they tend to per-

sist for longer periods in sediments, mainly under anaerobic

conditions (Knutzen, 1995). The toxicity of PAH is relatedto their speciation and, Todos os Santos Bay, it would be ex-

pected to be high, because it is presumed that petroleum de-

rived-PAH, which are present in solution or finely dispersed,

are more available to organisms and have higher toxicity

than soot-derived PAH (Knutzen, 1995). The negative partial

correlation obtained between the An/178 and the number of

species could be related to the fact that lower molecular

weight and more soluble PAH are bioaccumulated by marine

organisms from sediments and interstitial waters in greater

amounts than high molecular weight compounds (Baumard

et al., 1998). Is relevant to highlight that is not possible to ob-

tain this kind of information without combining aliphatic and

polycyclic aromatic hydrocarbon indices and concentration ra-tios with benthic ecological parameters.

Potentially adverse environmental conditions for benthic

fauna were previously reported at the stations located in the

centre and in the east region of the study area (Venturini and

Tommasi, 2004). At these places several individual PAH are

present in excess of the Sediment Quality Guidelines

(SQGs) values (based on McDonald et al., 1996; Long et al.,

1995), suggesting the occurrence of toxic biological effects.

In contrast, other stations seem to have fewer adverse condi-

tions for the establishment and development of benthic organ-

isms (Venturini and Tommasi, 2004). The observed decrease

in mean macrofauna density, number of species and diversity(ShannoneWiener index) from groups III to I seems to be re-

lated to the occurrence of high aliphatic hydrocarbon and PAH

concentrations associated with fine sediments. The introduc-

tion of organic contaminants such as petroleum hydrocarbons

to the marine environment can stimulate a high abundance of

some tolerant species or the extinction of the more sensitive

ones, due to the high toxicity of some compounds (Hyland

et al., 2000). In general, our results suggested the impoverish-

ment of the benthic community structure at group I relative to

group III, while group II showed intermediate characteristics.

PAH have detrimental effects on size and reproductive po-

tential of polychaete populations; however, some species are

able to degrade and excrete these compounds (Forbes et al.,

1996). The fact that Polychaeta was the dominant macro-

benthic group within the study area may be related to this ca-

pacity. Among Polychaeta the most abundant species were

Sigambra grubii and Dasybranchus cf. platyceps in group I,

Glycinde multidens in group II and Ophelina sp. in group III

due to its high density at station 3 as stated before. In addition,

Goniada littorea and Nematonereis schmardae were sub-dom-

inant in group III. Particle size, together with a complex of

factors that co-vary with it, would be responsible for the con-

trol of benthic communities’ composition. Capitellid poly-

chaetes are generally known as non-selective deposit-feeder

species associated with organically enriched areas (Frouin,




2000). Although the capitellid Dasybranchus cf. platyceps was

not dominant in Todos os Santos Bay, it was mainly recorded

at those stations with fine sediments and high hydrocarbon

concentrations. Moreover, cirratulid species (like Adouina

sp.) and Orbiniidae of the genera Scoloplos (like Scoloplos

treadwelli) found in this study and more abundant in group

II and I, respectively, are also characteristic species of sedi-ments with high organic content (Pearson and Rosenberg,

1978). On the other hand, the carnivorous polychaete Goniada

littorea was well represented in group III (excepting at station

3 were Ophelina sp. dominated). It was more abundant at sta-

tions 1, 2, 3 and 4 located near the mouth of Caıpe and Mat-

aripe rivers with the predominance of sandy sediment and low

organic content. The subsurface deposit-feeder Ophelina sp. is

a slender torpedo-shaped burrower opheliid commonly found

in sandy sediments (Fauchald and Jumars, 1979). Nematoner-

eis schmardae, the other sub-dominant species in group III, is

a subsurface deposit feeder polychaete, which was more abun-

dant at stations 15 with relatively higher aliphatic and UCM

contents than the other stations of this group.Molluscs had a small representation in Todos os Santos Bay.

The most abundant species were the filter-feeding bivalves

Chione cancellata in group I with high hydrocarbon concentra-

tions, andCorbula caribaea in group II with intermediate hydro-

carbon concentrations. According to Baumard et al. (1998),

filter-feeding bivalves are mainly exposed to the soluble and

more bioavailable fraction of PAH. Due to the occurrence of pe-

troleum-derived PAH present in solution or finely dispersed, the

uptake and exposure to harmful PAH for these two species is

supposed to be high within the study area. However, their occur-

rence at these groups of stations may be related to their limited

capacity to metabolise PAH. Effects of PAH on organisms areoften initiated through biotransformation of the compounds to

toxic metabolites, mainly by activation of the cytochrome

P450 enzymes. Generally, not considering interspecies varia-

tion, the capacity to metabolise PAH is best developed in fish,

intermediate in crustaceans and least in molluscs (Knutzen,

1995). Therefore, they would be more protected against cancer

induced by PAH metabolites and can accumulate PAH without

apparent damaging effects (Law and Biscaya, 1994).

Crustaceans had a minor representation within the study

area and a high number of species occurred at the stations

of group III characterised by less stressful conditions. In gen-

eral, crustaceans, especially amphipods, are more sensitive to

adverse environmental conditions such as organic enrichment,

oil and heavy metal contamination than Polychaeta (Grall and

Glemarec, 1997). Based on this characteristic the polychaete/

amphipod ratio has been used as a good indicator of environ-

mental impact (Dauvin and Ruellet, 2007). Even though this

ratio was not calculated, the two amphipods recorded in this

study Leucothoe spinicarpa and Heterophoxus videns were ab-

sent at the most impacted stations of group I, where opportu-

nistic polychaetes such as Sigambra grubii and Dasybranchus

cf. platyceps showed high relative abundances. Nevertheless,

tolerance to contaminants could vary among different groups

and among different species within a particular group (Knut-

zen, 1995) and crustaceans have been found at organically

enriched sites (Frouin, 2000). The presence of decapods of

the genera Alpheus exclusively at stations of groups I and II

with high hydrocarbon concentrations, could be related to

the living strategy of these organisms. According to Frouin

(2000) the construction of galleries by Alpheus together with

the animal displacement through them could reduce the expo-

sure of these decapods to contaminants, making possible theiroccurrence even at impacted sites. The distribution of sedi-

ment particles and particle-associated contaminants in marine

benthic environments results from the interaction of different

processes such as physical mixing, degradation and bioturba-

tion (Caradec et al., 2004). Moreover, borrow irrigation in-

creases interstitial water circulation and oxygenation of

sediments, which in turn could enhance the remobilisation

and degradation of previously buried hydrocarbons and im-

prove overall bottom conditions.

6. Conclusion

Our results showed that macrobenthic communities in the

northeast portion of Todos os Santos Bay are subjected to

the impact of chronic oil pollution. This fact was reflected

by profound changes observed such as species and diversity

reduction, mainly in the centre and in the east region of the

area. These results emphasise the importance of performing

multivariate approaches combining chemical data (indices,

concentration ratios and specific compound concentrations)

with biological information to improve the assessment of an-

thropogenic impacts on marine ecosystems.

Acknowledgements

We thank the colleagues from the FUNDESPA (Fundac~ao

de Estudos e Pesquisas Aquaticas) for their help in different

stages of this work. The Conselho Nacional de Desenvolvi-

mento Cientıfico e Tecnologico (CNPq) of the Brazilian Gov-

ernment is acknowledged for the MSc grant to N.V. This work

was developed within the project ‘‘Diagnostico Ambiental

Marinho da Area de Influencia da Refinaria Landulpho Alves,

Mataripe, Baıa de Todos os Santos’’ a partnership between

FUNDESPA and PETROBRAS (Petroleo do Brasil, SA). We

would like to thank M.Y. Yoshinaga for his comments and

for correcting the English. The manuscript was improved by

comments from two anonymous reviewers.

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