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Environmental Pollution 158 (2010) 1561–1569

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Environmental Pollution

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Large-scale risk assessment of polycyclic aromatic hydrocarbons in shorelinesediments from Saudi Arabia: Environmental legacy after twelve years of the Gulfwar oil spill

Adriana C. Bejarano*, Jacqueline MichelResearch Planning Inc., 1121 Park St., Columbia, SC 29201, USA

Risk Assessment of PAHs in shoreline sediments 12 years after the Gu

lf War oil spill.

a r t i c l e i n f o

Article history:Received 27 March 2009Received in revised form9 December 2009Accepted 11 December 2009

Keywords:PAH sediment toxicityPAH risk assessmentOil weatheringSaudi Arabia shoreline habitatsGulf war oil spill

* Corresponding author. Tel.: þ1 803 254 0278; faxE-mail address: ABejarano@researchplanning.com

0269-7491/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.envpol.2009.12.019

a b s t r a c t

A large-scale assessment of polycyclic aromatic hydrocarbons (PAHs) from the 1991 Gulf War oil spill wasperformed for 2002–2003 sediment samples (n ¼ 1679) collected from habitats along the shoreline ofSaudi Arabia. Benthic sediment toxicity was characterized using the Equilibrium Partitioning SedimentBenchmark Toxic Unit approach for 43 PAHs (ESBTUFCV,43). Samples were assigned to risk categoriesaccording to ESBTUFCV,43 values: no-risk (�1), low (>1–�2), low-medium (>2–�3), medium (>3–�5)and high-risk (>5). Sixty seven percent of samples had ESBTUFCV,43 > 1 indicating potential adverseecological effects. Sediments from the 0–30 cm layer from tidal flats, and the >30–<60 cm layer fromheavily oiled halophytes and mangroves had high frequency of high-risk samples. No-risk samples werecharacterized by chrysene enrichment and depletion of lighter molecular weight PAHs, while high-risksamples showed little oil weathering and PAH patterns similar to 1993 samples. North of Safaniyasediments were not likely to pose adverse ecological effects contrary to sediments south of Tanaqib.Landscape and geomorphology has played a role on the distribution and persistence in sediments of oilfrom the Gulf War.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

During the 1991 Gulf War an estimated 10.8 million barrels ofcrude oil were intentionally released into the Arabian Gulf (Tawfiqand Olsen, 1993). The oil was transported south by northwestwinds and regional circulation patterns, impacting virtually theentire Saudi Arabian shoreline from the Saudi-Kuwait border toAbu Ali Island, a distance of nearly 800 km (Gundlach et al., 1993).Studies one year after the spill showed little oil impact to subtidalhabitats, but extensive contamination of intertidal habitats, withdeep oil penetration into the abundant burrows, and 75–100% oilcoverage of extensive tidal flats as wide as 2 km (Hayes et al., 1993;Michel et al., 1993). Studies between 2002 and 2007 foundevidence of some recovery (RPI, 2003; Michel et al., 2005; Barth,2002, 2007); however, much of the intertidal habitat remainsseverely contaminated and natural recovery will likely take manydecades. The scale of impact from this spill, the largest in history, isunprecedented in scale and duration. In 2002–2003, a compre-hensive shoreline survey was conducted as part of the Kingdom of

: þ1 803 254 6445.(A.C. Bejarano).

All rights reserved.

Saudi Arabia’s claim for environmental damages resulting from thewar; there were large volumes of oiled sediments and habitatsaffected, even 12 years after the spill (Table 1).

Evidences from large-scale oil spills have shown that oil canpersist in coastal sediments for several decades and have long-termeffects on aquatic ecosystems (Burns et al., 1994; Peterson et al.,2003; Reddy et al., 2002; Short et al., 2004). Even in the absence ofacute toxicity, oil persistence in sediments can induce long-termecological effects through complex biological interactions (Peter-son et al., 2003; Southward et al., 1982). The bioavailable oil frac-tions can cause chronic sub-acute toxicological effect (poor health,reduced growth and reproduction, low recruitment rates), whichcan alter population dynamics and disrupt trophic interactions andthe structure of natural communities within ecosystems (Petersonet al., 2003). Slow ecological recovery also results from the physicaleffects of oil residues: presence of thick oil layers in marshes (Bakeret al., 1993), changes in soil compaction (Barth, 2007), and forma-tion of asphalt pavements that harden the sediment surface (Hayeset al., 1993).

Because natural recovery has been slow, the Kingdom of SaudiArabia is developing a plan to remediate the coastal habitatsaffected by the Gulf War oil spill. One component of the screening

Table 1Comprehensive shoreline survey (2002–2003) of intertidal habitats in Saudi Arabiabetween Kuwait and Abu Ali Island impacted by the 1991 Gulf War oil spill (RPI,2003).

Intertidalhabitat

Total area(km2)

Oiled area (km2)(Percent oiled)

Estimate of volumeof oiled sediments (m3)

Sand Beach 9.6 6.5 (57%) 880,150Tidal Flat 215.7 NA 5,221,000Salt Marsh 21.8 13.5 (62%) 1,804,000Mangrove 0.6 NA 80,650

A.C. Bejarano, J. Michel / Environmental Pollution 158 (2010) 1561–15691562

process is to evaluate the potential toxicological risks fromcontaminated sediments. During the 2002–2003 oiled shorelinesurvey conducted to support claims for direct environmentaldamages to the United National Compensation Commission, 2286sediment samples were analyzed for polycyclic aromatic hydro-carbons (PAH). Because sediment toxicity was not directly quanti-fied, we employed the Equilibrium Partitioning SedimentBenchmark Toxic Unit (ESBTU) approach for PAH complex mixtures(Di Toro and McGrath, 2000; USEPA, 2003). This approach quan-tifies the contribution of each PAH to the overall mixture toxicity,and is based on narcosis theory. Our goal was to use this existingdataset to identify and prioritize areas for further evaluation forremediation. In addition, analysis of these data provides docu-mentation of the impacts of the world’s largest oil spill on sedimentquality and oil-weathering rates in an arid, temperate setting in theabsence of shoreline cleanup efforts.

2. Materials and methods

2.1. Sediment sampling and chemical analysis

The design specified by the Kingdom of Saudi Arabia for the 2002–2003 oiledshoreline survey consisted of 3107 transects established at 250 m intervals from theKuwait border to Abu Ali Island. Along each transect, which extended across theintertidal zone (i.e., up to 2 km wide), pits were dug at 5–80 m spacing followinga systematic process for a total of 19,515 pits. The presence and thickness of surfaceand subsurface oil in each pit was recorded using standard visual oiling descriptions(NOAA, 2000) of No Visible Oil (NO), Lightly Oiled Burrows (LOB), Lightly OiledResidues (LOR), Moderately Oiled Burrows (MOB), Moderately Oiled Residues(MOR), Heavily Oiled Burrows (HOB) and Heavily Oiled Residues (HOR). Habitat typewas also recorded; we collapsed a more detailed classification into sand beach, tidalflat, oiled halophyte (less than 67% of the vegetation dead), heavily oiled halophyte(more than 67% of the vegetation dead), and mangrove (Avicennia marina). Halo-phytes were dominated by the perennial species Arthrocnemon macrostachyum andHalocnemon strobilaceum, and the annuals Salicornia herbacea and Suaeda. Sedimentsamples were systematically collected from individual oiled layers, as well asoverlying and underlying layers of ‘no visible’ oil. This specified sampling protocollead to an approximate 2:1 ‘no visible’ to ‘visible oil’ samples. All 26,158 sedimentsamples were analyzed for total petroleum hydrocarbons (TPH) using an AcceleratedSolvent Extraction procedure, followed by activated silica cleanup to remove non-hydrocarbon polar compounds and gravimetric analysis. Analysis of PAH andbiomarkers was performed on w10% of samples, with the goal of having one PAHanalysis per transect. Within oiling descriptors, frequency of samples for PAHanalysis was representative of TPH samples (paired t-test, p > 0.05), indicating lackof strong collection bias for a particular oiling descriptor. Target PAH and alkylatedPAH compounds were measured by GC/MS/SIM with a modified EPA method 8270(Page et al., 1995). PAHs analyzed (ng g�1, dry weight) included all 34 EPA priorityPAHs plus biphenyl, dibenzofuran, the dibenzothiophene homologue series (C0–C4

compounds), and C2–C3 fluoranthene/pyrene, for a total of 43 PAHs. Biomarkersincluded 18a- trisnorhopane and 17a- trisnorhopane. Total organic carbon (TOC; %,dry weight) was quantified in nearly 80% of the samples collected for PAH andbiomarker analysis. TOC analysis was performed by acidification to remove inor-ganic carbon followed by dry combustion and coulometric detection of the evolvedCO2.

2.2. Source of PAHs in Saudi sediments

Hopanoid biomarkers (18a- trisnorhopane (Ts) and 17a- trisnorhopane (Tm))were used to compare visibly oiled samples with suspected oil sources. Thesebiomarkers are ideal for source identification because of their stability and resis-tance to degradation. Oil Ts and Tm values were compared to values previouslyquantified across multiple Middle Eastern crude oils, including the likely sources of

the oil spilled during the 1991 Gulf War (Sauer et al., 1993a,b, EESAL, 2002; PME,2002; RPI, 2003). Samples collected during the 1992 R/V Mt. Mitchell Leg II scientificexpedition that investigated the impacts of the Gulf War oil spills on coastal andmarine environments of the Arabian Gulf were used to verify the oil source of thesediments analyzed here.

2.3. PAH toxicity assessment

We assessed the potential toxicity of these sediments with the EquilibriumPartitioning Sediment Benchmark Toxic Unit (ESBTU) approach for PAH complexmixtures (Di Toro and McGrath, 2000; USEPA, 2003). This approach is based on theequilibrium partitioning theory which states that, at equilibrium, nonionic organicchemicals in sediments partition between the organic fraction, interstitial water,and benthic organisms, where their affinity for organic carbon is a function ofchemical-specific organic partition coefficient (KOC). Based on narcosis theory (DiToro et al., 2000), the toxicity of individual PAHs in sediments can be predicted fromits octanol–water partitioning coefficient (KOW), a proxy for the affinity of chemicalsfor lipids. Di Toro et al. (2000) demonstrated that the slope of the acute toxicity ofindividual PAHs (Log (LC50)) and their Log (KOW) was practically the same acrossseveral aquatic species (i.e., universal narcotic slope). Thus, PAH-specific final acutechronic value (FCVi) can be estimated from the universal narcotic slope(m ¼ �0.945), the PAH-specific KOW, and the acute-to-chronic ratio from water-onlyacute and chronic toxicity tests (FCV ¼ 2.24 mmol g�1 octanol). This relationship isdescribed by FCVi (umol/L) ¼ 10^ (m * Log10KOW þ Log10FCV). The effects concen-tration of a specific PAH (COC, PAHi, FCVi) on an organic carbon basis can be calculatedfrom its estimated FCVi and KOC as COC, PAHi,;FCVi (mg goc

�1) ¼ FCVPAHi * KOC (USEPA,2003). The ESBTU for each PAH in the sediment sample (ESBTUFCVi) is then calcu-lated by dividing the organic carbon normalized PAH dry weight concentration inthe sediment sample (COC) by the COC, PAHi, FCVi. This benchmark approach wasoriginally designed for 34 priority PAHs, thus methods were modified to include allPAHs analyzed here. Under the assumption of narcosis as the predominant mode ofPAH toxicity, and additive toxicity of coexisting PAHs, ESBTU of the 43 PAHs in themixture (ESBTUFCV,43) were summed to generate a composite sediment toxicityestimate. ESBTUFCV,43 values greater than one suggests that the concentration of thePAH mixture in sediments may be unacceptable for the protection of sensitivebenthic organisms (USEPA, 2003). For estuarine and marine sediments, the USEPAguidelines recommend the use of the maximum solubility limit PAH concentration(COC, PAHi, MAxIi) to account for salinity effects on PAH solubility (ie., when COC, PAHi,

FCVi > COC, PAHi, MAxIi use COC, PAHi, MAxIi to calculate ESBTUFCVi). However, theconcentration of individual PAHs in these sediments was not sufficiently high toconstrain solubility.

Sediment toxicity was characterized by assigning each sediment sample toa ‘risk’ class according to its ESBTUFCV,43 value. This classification was defined asfollows: no-risk (ESBTUFCV,43 � 1), low-risk (ESBTUFCV,43 > 1-� 2), low to medium-risk (ESBTUFCV,43 > 2-� 3), medium-risk (ESBTUFCV,43 > 3-� 5), and high-risk(ESBTUFCV,43 > 5). Analysis of sample distribution within this risk classificationfocused primarily on the bulk of sediment samples with visible oil (oil classificationsLOB to HOR). TPAH comparisons were made across habitats via analysis of variance(ANOVA) followed by the Tukey–Kramer HSD (honestly significant difference forgroup means with unequal sample sizes) post-test for all pairwise comparisons(Kramer, 1956; Zar, 1999). TPAH concentrations were log transformed and tested fornormality and homogeneity of variance using the Shapiro–Wilk goodness-of-fit testand the Levene test, respectively. To assess potential sediment toxicity with depth,the samples were assigned to three sediment depths below surface: 0–30 cm, >30–<60 cm and �60 cm according to their recorded bottom depth.

2.4. PAH toxicity and oil weathering

An important matter relevant to this large-scale study is whether potentialtoxicity varies according to the degree of oil weathering in sediments. Thus, oilweathering was characterized by analyzing the ratios of specific PAH groups relativeto chrysenes, which are more resistant to weathering. Three PAH groups wereselected as their relative concentration in oil reflects different stages of oil weath-ering: naphthalenes (2-rings), phenanthrene/anthracenes (3-rings), and dibenzo-thiophenes (2-rings fused to a central thiophene ring). Double ratios were plottedfor each PAH group versus chrysenes (PAH group:TPAH (%) vs. chrysenes:TPAH (%)),using sediment samples assigned to opposite ends of the risk classification (no-riskand high-risk). The naphthalene, phenanthrene/anthracene, dibenzothiophene, andchrysene series included the parent compound plus C1–C4 homologues. Mean ratiodifferences between risk classifications and habitats were assessed with pairedStudent t-test, while differences across habitats assessed by ANOVA followed byTukey–Kramer HSD post-test for all pairwise comparisons. All variables were testedfor normality and homogeneity of variance using the Shapiro–Wilk goodness-of-fittest and the Levene test, respectively. Variables failing the homogeneity of variancetest were analyzed via the nonparametric Kruskal–Wallis Ranks test followed by thenonparametric Dunn’s test (for unequal sample sizes) post-test for all pairwisecomparisons (Glantz, 1988; Zar, 1999). Samples from the R/V Mt. Mitchell expeditionwere used to compare 1992 vs. 2002–2003 weathering patterns.

Fig. 1. Identification of PAH oil sources in intertidal sediments along the Saudi ArabianGulf shoreline via Tm/Ts ratios (n ¼ 1344). The gray shaded area brackets the Tm/Tsrange of the likely oil sources. The open circles represent Tm/Ts ratios of sedimentscollected one year post-spill (n ¼ 34); the black circles represent Tm/Ts ratios of Saudiand Iranian oils produced in the Gulf (Sauer et al., 1993a,b). Modified from RPI (2003).

A.C. Bejarano, J. Michel / Environmental Pollution 158 (2010) 1561–1569 1563

2.5. Sediment toxicity spatial visualization

Spatial clustering of no-risk to high-risk samples were generated by creatinga spatial weights matrix based on the Getis-Ord Gi* (Ord and Getis, 1995) usinga distance threshold of 2000 m. The Gi* statistics identify areas where samples withhigher-than-average (hot-spots; Z score>1.96) or lower-than-average (cold-spots; Zscore <1.96) risk levels tend to cluster together. Data visualization was enhanced byperforming a Kernel density analysis on the resulting G* statistics of each statisti-cally significant sample. To generate a one-dimension Gi* statistic, analyses wereperformed on the sample assigned to the highest risk class per pit. These analyseswere performed using the ArcGIS 9.3 spatial statistics toolbox (ESRI�, Redlands, CA).

3. Results

3.1. Source of PAHs in Saudi sediments

Sediment samples collected outside the oiled area (i.e.,comparison sites; n ¼ 27) were used to determine the backgroundTPAH concentration for the study area. Ninety-five percent of thesesamples (n ¼ 26) had TPAH concentrations � 511 ng g�1, indicatingthat a 500 ng g�1 TPAH is an appropriate upper limit backgroundconcentration. 17a- trisnorhopane (Tm): 18a- trisnorhopane (Ts)ratios of samples with ‘visible oil’ and TPAH >500 ng g�1 were usedto verify the source of oil contamination. Ninety-three percent(n ¼ 1254) of the samples collected in coastal and marine habitatsfor which Tm and Ts were simultaneously quantified fell within theTm/Ts range (2.67–3.74; Fig. 1) of likely oil sources of the 1991 spills(Kuwait, Tanagib, and Mardumah crude oils, oil from recovery pits;Sauer et al., 1993b; RPI, 2003). Nearly 60% (n ¼ 20) of a subset ofsediment samples collected one year following the spill during theR/V Mt Mitchell-ROPME expedition (Hayes et al., 1994) also fellwithin the Tm/Ts range of the likely oil sources. These findingsconfirm that the great majority of sediments collected in thecurrent study were contaminated with 1991 oil sources.

Table 2TPAH concentrations by risk categories from samples collected across habitats and oiling

Risk classification ESBTUFCV,43 Sample size PAH con

Mean �

No-Risk �1 558 601 �Low >1–�2 140 2781 �Low-Medium >2–�3 79 4633 �Medium >3–�5 88 7359 �High >5 832 90,570 �a BDL ¼ Below detection limit.b Effects Range Low (ERL) and Effects Range Median (ERM) represent the 10th and 50t

cause adverse ecological effects (Long et al., 1995).

3.2. PAH toxicity assessment

ESBTUFCV,43 values were calculated for 2072 samples. Totalorganic carbon (TOC; %, dry weight) was measured in 80% of thesamples collected for PAH analysis; however, a regression analysis(data not shown) suggested that the presence of oil increased theamount of TOC in sediments (r2 ¼ 0.7, p-val <0.0001). To correct forthe potential oil bias on sediment organic carbon, the median TOCfrom all ‘no visible oil’ (NO) sediment samples (TOC ¼ 0.205%;n ¼ 220) was used in ESBTUFCV,43 calculations. The great majority ofsamples with ‘no visible oil’ (97.5%; n ¼ 365) had ESBTUFCV,43 � 1indicating that the visual classification performed well. By contrast,only 33% percent (n ¼ 558) of the samples with visible oil had ESB-TUFCV,43 values � 1. ESBTUFCV,43 values in potentially toxic samplesranged from >1 to 928, although most samples (95%) hadESBTUFCV,43 < 150. In lightly oiled sediments, TPAH concentrations(pooled LOB and LOR ¼ 4467 � 10,373 ng g�1) were significantlydifferent from moderately oiled sediments (pooled MOB andMOR ¼ 12,274 � 43,014 ng g�1; p < 0.0001). TPAH concentrationdifferences were also found between HOB and HOR(72,709� 80,482 ng g�1 and 122,475�124,999 ng g�1, respectively;p < 0.0001), and between these two oil descriptors and lightly andmoderately oiled sediments.

In order to characterize sediment toxicity of ‘visibly oiled’ (LOBto HOR; n ¼ 1679) samples by habitat, each sample was assigned toa risk class according to its ESBTUFCV,43 value (Table 2). This riskclassification can be compared to the sediment quality guidelines ofLong et al. (1995): the Effects Range Low (ERL ¼ 4022 ng g�1, dryweight) and Effects Range Median (ERM ¼ 44,792 ng g�1, dryweight). The ERL and ERM represent the 10th and 50th percentilesof PAH concentrations in sediment found in the scientific literatureto cause adverse ecological effects (Long et al., 1995). Over half(56%) of the sediments were described as moderately oiled, 28%were described as heavily oiled, and 16% were described as lightlyoiled. Mean TPAH concentration in the high-risk class was one andtwo orders of magnitude larger than the medium and no-riskclasses, respectively. The distribution of the five risk classes byoiling descriptor is shown in Fig. 2. A large proportion of sedimentsdescribed as LOB (67%) and LOR (67%) are predicted to be non toxic,while most HOB (82%) and HOR (87%) samples would pose high-risk of toxicity. Sediments described as either MOR or MOB hasa much wider range of toxicity, with peaks at both high-risk andno-risk. Clearly, sediments described as either HOR or HOB containmostly toxic levels of TPAHs, while sediments described as eitherLOR or LOB do not.

Across habitats and within the high-risk class, beaches hada significantly higher mean TPAH concentration (112,983 �139,316 ng g�1; p ¼ 0.002) compared to tidal flats, oiled halophytes,and heavily oiled halophytes (pooled mean 76,419 � 83,907 ng g�1;Fig. 3A). No other TPAH differences across habitats were found withinthe remainder risk classes. Elevated mean TPAHs in high-risk beachsediments reflect the relatively larger proportion of samples assigned

descriptors.

centration (ng g�1, dw) Mean sample TPAH relative to Guidelineb

sd (min–max)

546 (BDLa�2202) <<ERL540 (1820–3995) <ERL585 (3235–5786) wERL1175 (3661–9624) >ERL-<ERM110,163 (9349–1,556,888) �ERM

h percentiles of PAH concentrations in sediment found in the scientific literature to

Fig. 2. Frequency distribution of risk classes by oiling descriptor. Lightly Oiled Burrows(LOB), Lightly Oiled Residues (LOR), Moderately Oiled Burrows (MOB), ModeratelyOiled Residues (MOR), Heavily Oiled Burrows (HOB), and Heavily Oiled Residues (HOR).

No-risk High-risk

Naphthalenes 0.84 � 2.23% 5.57 � 5.76%Phenanthrene/anthracenes 4.62 � 5.83% 13.87 � 4.10%Dibenzothiophenes 16.79 � 18.31% 57.11 � 8.83%Chrysenes 38.58 � 15.13% 9.83 � 6.29%

A.C. Bejarano, J. Michel / Environmental Pollution 158 (2010) 1561–15691564

to the visual oil descriptor with the highest TPAHs, HOR (56% of totalsamples; Fig. 3B). By comparison, HOR samples comprised between12% and 27% of the total high-risk class samples in the remainderhabitats. Heavily oiled halophytes had the largest number of oiledburrow samples assigned to the high-risk class (MOB ¼ 29% andHOB ¼ 47%), followed by oiled halophytes (HOB ¼ 29%), while bea-ches had the lowest frequency (MOB¼ 3% and HOB¼ 4%), reflectinga high density of burrowing crabs in marshes.

Samples assigned to each risk class were analyzed based ontheir sediment depths: 0–30 cm, >30–<60 cm and �60 cm (Fig. 4).Eighty-five percent (n ¼ 1436) of all samples were collected withinthe top 30 cm of the sediment layer. Thirty three percent of these(n ¼ 558) were classified as posing no-risks to benthic organisms,while 49% (n ¼ 832) were classified as posing a high-risks. Withinhabitats, mangroves had the highest frequency of samples from thetop 30 cm classified as no-risk (69%, n ¼ 9), whereas beaches hadthe lowest frequency (25%, n¼ 162). Comparing halophyte habitats,oiled halophytes had 57% (n¼ 74) of the samples categorized as no-risk, whereas heavily oiled halophytes had 29% (n ¼ 22). Tidal flatshad the largest frequency of samples in the top 30 cm assigned tothe high-risk class (51%), followed by beaches (31%) and heavilyoiled halophytes (28%). Across all habitats, most samples collectedat >30 cm depth (>81%) were assigned to the high-risk class.Compared to other habitats, mangroves and heavily oiled halo-phytes had a higher frequency of high-risk samples in the >30–<60 cm sediment range (15% and 17%, respectively), reflecting thepresence of deep oiled burrows in the upper intertidal zone. Only

beaches had sediments samples collected at �60 cm depth, cor-responding to 4% (n ¼ 61) of all the samples. Of these 61 samples,nearly 60% were categorized as posing high toxicological risks.

3.3. Toxicity and oil weathering

In order to assess the relationship between oil weathering andsediment toxicity, analyses were performed for samples on oppo-site ends of the risk classification (no-risk and high-risk) andrelative to specific PAHs. Only samples with TPAH concentrationsabove background (>500 ng g�1) and within Tm/Ts ratios of thelikely oil sources were included in the analysis (see Fig. 1). Thepercent of each PAH group for the two end-member risk classeswere as follows:

Double-ratio plots (Fig. 5) show the transition in oil weatheringfrom naphthalenes to dibenzothiophenes relative to chrysenesbetween these two risk classes. The naphthalenes vs. chrysenes plotshows no-risk samples dominated by a low percent of naphthalenes(<7% of the TPAHs in 97.5% of the samples) but relatively enrichedwith chrysenes (up to 87% of the TPAHs). These results are consis-tent with the loss of the more volatile and soluble naphthalenesduring early stages of oil weathering. By contrast, the high-riskgroup had relatively larger amounts of naphthalenes (up to 29% ofthe TPAHs) and smaller amounts of chrysenes (�26% of the TPAHs in97.5% of the samples). Mean naphthalenes to chrysenes ratios in thehigh-risk samples (1.2 � 1.74) were on average forty times largerthan those of no-risk samples (0.03 � 0.07). A clearer separationbetween these two risk classes is evident in the plots with thehigher molecular weight PAHs phenanthrenes–anthracenes anddibenzohiphenes. In the no-risk group, phenanthrenes-anthracenescomprise 0–28% of the TPAH (<12% of the TPAHs in 90% of thesamples), while in the high-risk group most of the samples (95%) arelumped between 8% and 25% phenanthrenes–anthracenes and<30% chrysenes. Phenanthrenes-anthracenes to chrysenes ratios inhigh-risk samples (2.07 � 1.37) were nearly nine times larger thanthe no-risk samples (0.24 � 0.53). In the dibenzothiophenesplot, this group of PAHs comprise 44–79% of the TPAHs in 90% of thehigh-risk samples, clearly grouped at<30% chrysenes. Although theno-risk samples are spread across the entire scale of the dibenzo-thiophenes, these samples are characterized by higher amounts ofchrysenes (30–50% of the TPAHs) and notably lower amounts ofdibenzothiophenes (<48% of the TPAHs in 90% of the samples) thanthe high-risk group. The results are consistent with later stages of oilweathering, where oil would be relatively enriched with chrysenesas the more degradation-resistant dibenzothiophenes are depleted.Dibenzothiophenes to chrysenes ratios in high-risk samples(8.73 � 5.66) were one order of magnitude larger than the no-risksamples (0.84 � 1.53). In all of these double-ratio plots, samplesfrom the R/V Mt Mitchell expedition (n¼ 32; TPAH>500 ng g�1 andTm/Ts ratios falling within the range of the likely source) match therelative PAH composition of the high-risk samples, suggesting thatthe oil in these sediments has not substantially weathered above theweathering observed one year post-spill.

The relative composition of naphthalenes, phenanthrenes-anthracenes, dibenzothiophenes and chrysenes, and PAH ratiosbetween the two risk classes and across habitats were also evalu-ated. PAH sample distribution was clearly different between the

Fig. 3. Habitat-specific total polycyclic aromatic hydrocarbon (TPAH) concentration (ng g�1, dry weight; mean � standard deviation) by risk class (A); and sample frequency byvisual oiling in the high-risk class only (B). Lightly Oiled Burrows (LOB), Lightly Oiled Residues (LOR), Moderately Oiled Burrows (MOB), Moderately Oiled Residues (MOR), HeavilyOiled Burrows (HOB) and Heavily Oiled Residues (HOR).

A.C. Bejarano, J. Michel / Environmental Pollution 158 (2010) 1561–1569 1565

two risk classes (shown for chrysenes in Fig. 6). Although sampledistribution across habitats showed similar patterns, there weresome significant differences in PAH ratios (Table 3). Within the no-risk class, all ratios were statistically different (analyzed withnonparametric tests) between beaches and tidal flats. PAH ratios inbeach samples were smaller than tidal flat ratios because of theirrelatively large proportion of chrysenes, and smaller amounts ofphenanthrenes-anthracenes, and dibenzothiophenes. These resultsmay indicate slightly higher oil weathering in beaches than in tidalflats. Within the high-risk class, naphthalene to chrysene ratioswere statistically different (analyzed with parametric tests)between heavily oiled halophytes and all other habitats. In heavilyoiled halophytes, naphthalenes were 56–60% higher, while chrys-enes 20–25% lower than in all other habitats. These results maysuggest slower weathering rates of naphthalenes from sediments

Fig. 4. Percent of oiled sediment samples by habitat and depth (cm) classified into riskcategories according to their ESBTUFCV,43 values.

in heavily oiled halophytes. Within the high-risk class, dibenzo-thiophene to chrysene ratios were statistically different betweenbeaches and tidal flats, reflecting larger proportion of chrysenes,and smaller amounts of dibenzothiophenes in beaches.

3.4. Sediment toxicity spatial visualization

The risk classification of samples was used to spatially visualizethe condition of sediments along the shoreline of Saudi Arabia.Clusters dominated by samples assigned to the no-risk class (cold-spots) dominated the northern portion of the Saudi coastline(Fig. 7). From Khafji to Safaniya, 68–100% of sample in the clusterswere classified as posing no-risks. In the three small bays of Khafji,Ras Mi’Shab, and Prince Sultan Beach Resort, 65–69% of the samplesin the clusters were classified as no-risk, while <20% were classi-fied as high-risk. From Safaniya to Tanaqib sediments were domi-nated by high-risk samples (55%), but samples were spread over ca.30 km where clear clusters were not identified. South of Tanaqibcoastal areas had sediment cold- and hot-spots, but hot-spots werehighly dominant. In the Tanaqib and Manifa areas 45% and 61% ofsamples in hot-spot clusters, respectively, were high-risk samples.From Manifa to north of Ras az Zawr, these mostly sand beachsediments were dominated by risk classes other than no-risk (63%),primarily high-risk samples (48%). However, samples were spreadover ca. 40 km where clear clusters were not identified, reflectingsporadic areas where heavily oiled sediments had been buried bylong-term accretion. South of Ras az Zawr, in the large shelteredbays of Musallamiyah and Dafi, the large majority of clusters werehot-spots dominated primarily by high-risk samples (53%).However, two cold-spot clusters were identified northeast andsouthwest of Dafi. The samples with the highest ESBTUFCV,43 values>100 were found between Tanaqib and Dafi.

Fig. 5. Relative abundance of naphthalenes, phenanthrenes-anthracenes and dibenzo-thiophenes versus chrysenes as indicators of the transition between early and latestages of oil weathering. The circles represent samples from the no-risk (white) andhigh-risk (black) classes; the squares show the composition of PAHs in sedimentscollected one year post-spill (n ¼ 34).

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4. Discussion

Intertidal sediments collected 12 years post-spill along theshoreline of Saudi Arabia unmistakably match the signature of thelikely oil sources demonstrating that sediments across coastal

Fig. 6. Percent chrysene distribution in samples from the no-risk and high-risk classesacross habitats.

habitats are still contaminated with oil from the Gulf War spills. Todate only one study assessed the toxicity of Saudi Arabian shorelinesediments. Two and a half years after the spill Randolph et al. (1998)showed that contaminated sediments between Tanajib and Abu Alicaused significant reduction in the survival of the marine amphipodRhepoxynius abronius, suggesting that sediments from the areaposed adverse toxicological effects to native benthic infauna. Theauthors suggested that sediment manipulation induced the loss oftoxic fractions, and that therefore in-situ toxicity was likely greaterthan observed under laboratory conditions. Our approach, using theEquilibrium Partitioning Sediment Benchmark Toxic Unit (ESBTU)method, showed that a large proportion of the samples (67%) maypose adverse ecological effects to benthic organisms. Of thosepotentially toxic samples, 73% were assigned to the high-risk class.TPAH concentrations in the high-risk class were similar to the levelsfound in sheltered areas one year after the oil spill (100,000–300,000 ng g�1; Hayes et al., 1993), indicating that there has beenlittle physical removal or microbial degradation of the oil in theseheavily oiled intertidal sediments.

Differences in the depth profile of potentially toxic sedimentsreflect intrinsic differences across habitats, where habitat-specificprocesses and geomorphology play a key role in oil distribution andpersistence. Tidal flats had the highest frequency of high-risksamples collected from the top 30 cm, while beaches, heavily oiledhalophytes, and mangroves had the highest frequency of high-risksamples collected from the >30–<60 cm layer. Beaches were theonly habitat with visually oiled sediments >60 cm, most of whichare predicted to be toxic. These differences primarily reflect thetidal elevation (i.e., tidal range z 1.3 m) and the nature of thepermeability of each habitat. Halophytes and mangroves arelocated in the upper and supra tidal zone; the sediments are mostlyfine-grained, and numerous crab burrows (on the order of20–100 m�2) are deep enough to reach the water table during lowtides. The extensive tidal flats are located from mid-tide to low tide,and the water table seldom drains below 25 cm. Most of thesamples were collected from the extensive sandy tidal flats wherethe oil was able to penetrate into the permeable surface sedimentsas well as into numerous burrows. On the muddy tidal flats, oilpenetrated into the numerous burrows, while on beaches, oilpermeated sediments forming continuous layers of oiled sedi-ments. In addition, half of the beaches in the study area haveundergone long-term accretion (up to 20 cm; RPI, 2003), which haslead to deep burial of the oiled sediments. These deeply buriedoiled layers are usually classified as HOR and highly toxic.

Physical removal processes have been effective only along theexposed outer beaches where 50% contained ‘no visible’ oil in2002–2003. Along moderately exposed sand beaches inside thebays, 41% contained ‘no visible’ oil. In contrast, only 15% of themuddy tidal flats and 35% of the halophytes contained ‘no visible’oil. The oiled sediments provided a ready marker by which tomeasure sedimentation on flats and halophytes. In the twelve yearssince the spill, the average total sediment accumulation was 0.6 cmfor halophytes and 0–1 cm for tidal flats (RPI, 2003), indicating thatin marshes and flats the oiled layers have been buried slowly.

Major changes in PAH composition occur during weathering ofoil, including enrichment of chrysenes relative to other PAHs, anddecrease in the ratios of specific PAH groups (naphthalenes, phen-anthrenes, dibenzothiophenes, and fluorenes) to the more weath-ered resistant chrysenes (Wang and Fingas, 2003). All double-ratioplots showed a separation between no-risk and high-risk samples,which was more evident with relatively more weather resistantPAHs. Double-ratio plots indicate that the least potentially toxicsediments have undergone some level of weathering (i.e., moderateto extreme), while the most potentially toxic sediments have notsubstantially weathered relative to 1992 samples. Sauer et al. (1998)

Table 3Specific PAH ratios (mean � standard deviation) across representative habitats for samples classified as posing no-risks (No) or high-risk (High). Within rows, habitatssharing the same letter are not significantly different from each other (a ¼ 0.05). N/C ¼ naphthalenes/chrysenes, P-A/C ¼ phenanthrenes–anthracenes/chrysenes, andD/C ¼ dibenzothiophenes/chrysenes.

PAH ratios Risk Beaches Heavily oiled halophytes Oiled halophytes Tidal flats

Sample size No 86 17 30 107High 286 33 24 409

N/C No 0.02 � 0.08a 0.005 � 0.02a,b 0.02 � 0.04a,b 0.043 � 0.09b

High 1.09 � 1.53a 2.11 � 2.16b 1.06 � 1.73a 1.21 � 1.83a

P-A/C No 0.09 � 0.21a 0.18 � 0.26a,b 0.18 � 0.28a,b 0.38 � 0.72b

High 1.91 � 1.27a 2.36 � 1.25a 2.37 � 1.22a 2.14 � 1.45a

D/C No 0.33 � 0.92a 0.65 � 0.88a,b 0.82 � 1.27a,b 1.28 � 1.91b

High 7.84 � 5.25a 10.16 � 4.9a,b 8.49 � 5.12a,b 9.24 � 5.25b

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evaluated oil weathering in sediments collected along the Saudicoastline between 1992 and 1993, and found the least amount ofweathering in subsurface sediments from moderately exposed sandflats and in sheltered muddy sediments with reduced exposure tophysical weathering processes. These sediments weretypically classified as moderately to heavily oiled and hadTPAH> 180,000 ng g�1. These concentrations are within the range ofthe high-risk class sediments presented here. Surface and subsurfacesamples from 1993 lost >80% and nearly 75%, respectively, of thenaphthalene (parent compound only) content of the stranded oil,while the most weathered samples had<10% naphthalenes. Samplesfrom 2002 to 2003 assigned to the no-risk and high-risk classesshowed relatively lower naphthalenes (mean 0.84% and 5.57%,respectively; parent compound plus C1–C4 naphthalene homo-logues) indicating that some weathering by evaporation and dilutionhas occurred, except for a few samples from both classes wherenaphthalenes were as high as 29%. Lack of enrichment of thechrysene series in the high-risk samples further indicates a lowerdegree of weathering compared to low-risk samples, revealing highpotential for sediment toxicity. These results further support the ideathat oil weathering reduces toxicity (Di Toro et al., 2007).

Barth (2003, 2007) showed that ten years after the oil spill, saltmarshes along the Saudi coast had the least amount of recovery.Delayed salt marsh and tidal flat recovery seems to be the result ofmultiple intertwined processes including the absence of physicalenergy (i.e., tidal flow and wave action), and the presence ofa highly anoxic and nutrient-depleted sediment environmentcaused in part by laminated cyanobacteria mats (dominated byMicrocoleus chthonoplastes and Lyngbya aestuarii; Barth, 2003;Berthe-Corti and Hopner, 2005; RPI, 2003). In 2002–2003, cyano-bacteria mats covered 20–40% of the oiled tidal flat and halophytehabitats compared to 0–8% cover in unoiled areas (RPI, 2003).Studies have documented the effects of these algal mats in slowingnatural recovery by forming a physical barrier that preventsgermination of seeds, settlement of larvae, tidal flushing, oxygenexchange, and bioturbation of infauna (Barth, 2003; Michel et al.,2005; Hopner and Al-Shaikh, 2008). These mats have hindered re-colonization by burrowing macrofauna, and prevented soil aerationand oil degradation, particularly in heavily impacted marshes.Increased bioturbation and increased density of crab burrowsbetween 1999 and 2002 along tidal channels caused destabilizationof the sediment surface, facilitating oil degradation and improvinghabitat quality (Barth, 2007). These observations explain thesignificantly higher naphthalenes to chrysenes ratios in high-risksamples from heavily oiled halophytes compared to other habitats.Cyanobacteria mats in this habitat likely prevented early oilweathering (loss of naphthalenes) through evaporation anddissolution. In one study, aliphatic and aromatic hydrocarbonswere preserved under these mats, with sediments a deep as 15 cmshowing low oil weathering (Garcia de Oteyza and Grimalt, 2006).

Although heavily oiled halophytes had relatively higher ratios ofthe other PAHs, differences were not statistically significantcompared to other habitats presumably because of the relativelysmall sample size and high variation. Other PAH ratio differencesbetween beaches and tidal flats were found within risk classes,highlighting latent differences in oil weathering between thesehabitats. In general, higher PAH ratios in tidal flats (except for N/Cand P-A/C in high-risk samples) indicate lower enrichment ofchrysenes, and perhaps lower oil-weathering rates. One cleardifference between these two habitats is the anoxic environmentand higher organic content in tidal flats (data not shown), andhigher sediment porosity and mechanical energy on beaches(Hayes et al., 1993). A large body of literature on oil spills in tropicalcoastal habitats has also shown the influence of habitat-specificproperties on oil degradation. Burns et al. (1993, 1994, 2000)demonstrated that in salt marshes, coarse sediments with largeramounts of sands and organic carbon facilitated oil degradationcompared to intertidal mangroves, and that in deep anoxicmangrove mud, hydrocarbons can persist for more than 20 years.The affinity of PAHs for the sedimentary organic carbon fraction(organic carbon–water partition coefficients) partially depends onthe size of the sediment particle, which determines the number ofbinding sites. Silt and clay are more highly charged than sand,allowing larger interactions with organic matter (de Brouwer et al.,2000) and therefore influencing PAH affinity (i.e., decreasing fromsilt to sand). High affinity of PAHs for organic carbon influencestheir partitioning into water and hinders their degradation.Although we suspect that particle size influences oil-weatheringrates, we did not analyze habitat-specific differences between fine(mud) and coarse (sand) sediments, primarily because of lack ofpower (i.e., small sample size with fine sediments).

Oil weathering in sediments depends on evaporation, dissolu-tion and removal of lower molecular weight constituents, andmicrobial degradation. These processes may be inherently differentacross habitats as they have unique physical and biological features.Even within habitats, spatial variables (i.e., prevailing currents,wave energy, landscape, and geomorphology) will likely influenceoil distribution and weathering. The impact of these variables isevident in the distribution along the coast of samples assigned toeach of the risk classes. Over half of the visibly oiled samplescollected north of Safaniya were classified as posing no-risks (66%)while relatively fewer (17%) were assigned to the high-risk class.Even the three small bays north of Safaniya (Khafji, Ras Mi’Shab,and Prince Sultan Beach Resort) had similar sample distributions(65%–69% no-risk and 13%–19% high-risk). The relative highabundance of no-risk samples in the area reflects differences ininitial oil loading as well as landscape changes between northernand southern portions of the coast. The northern area is dominatedby outer sand beaches where sediment reworking by wave actionhas eroded much of the oil. By contrast, the frequency of high-risk

Fig. 7. Spatially visualization of sediment condition along the shoreline of Saudi Arabia. Pie charts (top-left) show sample frequency distributions based on risk classes in threerepresentative areas. Maps of shoreline segments (A, B, C) within each of these three areas show spatial clustering of risk class samples based on cold- and hot-spot analysisenhanced with Kernel density estimation.

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samples increased south of Tanaqib particularly between Ras azZawr and Dafi. These areas, which received large oil loadings, arecharacterized by relatively sheltered bays with wide tidal flats. Ingeneral, the areas with the highest frequency of high-risk sampleswere typically located in moderately exposed and sheltered bays.

5. Conclusions

Twelve years after the Gulf War oil spill, sediments from coastalhabitats particularly along the southern portion of the shoreline ofSaudi Arabia, had PAH concentrations that may be unacceptable for

the protection of benthic fauna. This and other studies (Barth, 2002;RPI, 2003; Hopner and Al-Shaikh, 2008) indicate that coastal habi-tats in the study area have not recovered from the impacts of the1991 oil spill and that full recovery will take decades more. Thegovernment of Saudi Arabia will design and implement remediationstrategies to speed the rate of habitat recovery. The visible oilingdescriptions and the 2002–2003 sediment chemistry data will beused as part of the site-selection process; however, these data willneed to be validated with field surveys that will also update infor-mation on ecological condition. The analyses shown here (i.e., Fig. 7)could be incorporated into the screening process that will

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ultimately select sites for potential remediation. Managementdecisions regarding remediation strategies and locations will alsoinclude information on habitat type, degree of exposure, logisticalconstraints, accessibility, potential remediation methods, and like-lihood of success given site-specific characteristics.

Acknowledgements

The Oiled Shoreline Survey was sponsored by the Presidency forMeteorology and Environment, Kingdom of Saudi Arabia. We arethankful to the field teams that collected the samples under diffi-cult conditions. We also thank, M. O. Hayes and L. Cotsapas for theirleadership during the fieldwork, and G. Douglas who oversaw thechemical analysis.

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