Spatial and temporal changes in benthic communities of the Galician continental shelf after the Prestige oil spill

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Marine Pollution Bulletin 53 (2006) 315–331

Spatial and temporal changes in benthic communities of theGalician continental shelf after the Prestige oil spill

Alberto Serrano a,*, Francisco Sanchez a, Izaskun Preciado a,Santiago Parra b, Inmaculada Frutos b

a Instituto Espanol de Oceanografıa, P.O. Box 240, 39080 Santander, Spainb Instituto Espanol de Oceanografıa, P.O. Box 130, 15080 La Coruna, Spain

Abstract

Two years after the Prestige oil spill (POS) an assessment of the effects on benthic fauna was carried out using the data obtained in fivemultidisciplinary surveys. Otter trawl, beam trawl, suprabenthic sled and box corer were used to study the main benthic compartments,along eight transects perpendicular to the coastline. Beam trawl was also employed to quantify the amount of tar aggregates on the con-tinental shelf. No significant correlations between tar aggregates and species richness, biomass and diversity of benthic communities werefound. This result was corroborated when the role of depth, season, latitude and sediment characteristics was examined by canonicalordination, in which POS-related variables had low influence on spatial distribution patterns. Depth and sediment grain diameter pro-foundly influence epibenthic communities. Sediment organic content is a third key variable for the infaunal, suprabenthic and lower-sizedepibenthic communities, but not for the larger epibenthic communities. Nevertheless, a decrease in the densities of several epibenthicindicators was detected the first year after spill, followed by a noteworthy recovery in 2004. Non-macroscopic toxicity and some ocean-ographic agents are suggested as possible causes of these shifts.� 2005 Elsevier Ltd. All rights reserved.

Keywords: Prestige oil spill; Galician shelf; Tar aggregates; Benthic communities; Oil impact indicators; Canonical ordination

1. Introduction

The Prestige oil spill (POS) resulted in the release of over50 000 tons of heavy oil (type M-100) 250 miles from theGalician coastline in oceanic waters (Northwest IberianPeninsula) in November 2002. Following the POS, the oilwas dispersed and sank, mainly due to the bad winterweather conditions and wave action (Sanchez, 2003). Thisheavier fractions of oil reached the bottom by droppingfrom the water column as tar aggregates with low bioavail-ability or in the form of small toxic particles in sea snow.This toxic component of sea snow may have been madeup of degraded oil components and dead agglutinate

0025-326X/$ - see front matter � 2005 Elsevier Ltd. All rights reserved.

doi:10.1016/j.marpolbul.2005.09.030

* Corresponding author. Tel.: +34 942 291060; fax: +34 942 275072.E-mail address: [email protected] (A. Serrano).

planktonic organisms. Tar aggregates (with the Prestige

chromatographic fingerprint according to analysis of theIIQAB-CSIC of Barcelona) were found on the shelf onemonth after the spill, and there is evidence of a micropar-ticled sinking process in planktonic surveys taking placein the POS area in winter 2002, in which oil was found inthe exoskeleton and the gut of several zooplankton species(Bode et al., 2003). Oil drops and stains were also found insuprabenthic amphipods following the POS (Frutos andParra, 2004). Therefore, the shelf taxa initially affected bythose sedimented oil components are assumed to be sec-ondary producers, suspension feeders and detritivorousorganisms, followed by planktophagous and benthopha-gous organisms in the trophic web. These possible shiftsin the abundances of lower trophic levels would unleashcascading bottom-up type ecosystem effects (Petersonet al., 2003). In the Baltic, following the Tsesis spill, trophic

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Fig. 1. Location of sampling stations in the area affected by the prestigeoil spill (Galician Atlantic coast). Lines delimit zones with different impactlevels of tar aggregates: minimum impact (Zone 1), maximum impact(Zone 2) and medium impact (Zone 3).

316 A. Serrano et al. / Marine Pollution Bulletin 53 (2006) 315–331

oil transmission was detected to a benthophagous flatfish(Elmgren et al., 1983). Sturdevant et al. (1996) detectedchanges in the feeding habits of juvenile planktophagousfishes after the Exxon Valdez spill. Other bottom-up effectsinclude enhancement of hydrocarbon-degrading bacteria,oligochaete and deposit-feeding polychaetes by petroleumhydrocarbon enrichment (Peterson, 2001). This fact mayproduce enhanced production of demersal fishes or crusta-ceans of higher trophic levels.

On the other hand, top-down effects may also berelevant due to spatio-temporal prohibitions on trawlingfollowing the POS, which reduced fishing mortality(Punzon et al., 2005) and led to an enhancement in thebiomass of top predators that affected lower trophiclevels.

These cascading changes may affect benthic taxa in dif-ferent ways. Several sensitive or opportunistic taxa can beused as indicators. Benthic species of slow growth and withslow recovery capability, mainly crustaceans and echino-derms, show a high sensitivity to oil exposure. Several stud-ies have shown a fall in populations of sensitive species,such as benthic Ampeliscidae, crabs, gastropoda and echi-noderms (Dauvin, 1982; Elmgren et al., 1983; Feder andBlanchard, 1998; Gomez Gesteira and Dauvin, 2000; Peter-son, 2001). Furthermore, initial mortalities may be fol-lowed by extreme fluctuations of stress-tolerant oropportunistic species, such as capitellid or spionid poly-chaetes (Dauvin, 1982; Pearson and Rosenberg, 1978;Suchanek, 1993).

The epibenthic fauna of the Galician continental shelf iswell documented by the surveys carried out every autumnsince 1983 (Olaso, 1990; Sanchez et al., 2002; Sanchezand Serrano, 2003). These studies, which indicate a diversebenthic community, represent a good starting point formaking pre-spill and post-spill comparisons as well asfor analysing changes between minimum-impacted vsmaximum-impacted areas after the POS. Few studies havebeen carried out on the effects of hydrocarbons on shelfcommunities. Most describe effects less pronounced thanon intertidal ecosystems (e.g. Feder and Blanchard, 1998;Peterson, 2001) as the shipwrecks usually take place nearthe shoreline and the distribution of oil appears scatteredin the subtidal. The location of the Prestige wreck andthe oil trajectory over the shelf suggest greater effects onGalician shelf communities than have occurred in otherspills.

The present work approaches the study of these possibleeffects through a multigear sampling system, analysing var-iation in the spatio-temporal distribution of main benthiccompartments. The main goals were: (1) to analyse shiftsin the biomass and diversity of benthic communities amongareas of different impact; (2) to determine pre-spill andpost-spill changes in the shelf ecosystem; (3) to study vari-ations in sensitive taxa following the POS; and (4) to ana-lyse the relevance of tar aggregates on the abundance andcomposition of benthic communities following the POSin relation to other environmental variables.

2. Material and methods

2.1. Field sampling

The study area includes the Galician continental shelfbetween 70 m and 300 m depth. A total of eight transectsperpendicular to the coastline, with stations located at threedifferent depth strata (A: 70–120, B: 121–200, C: 201–300 m), were established (Fig. 1). Following the POS, fivesurveys were carried out in 2002, 2003 and 2004 (winter2002, spring 2003, autumn 2003, spring 2004 and autumn2004). Four samplers were used in order to study the differ-ent compartments of benthic fauna. Epibenthos was studiedusing two different gears, a Baca otter trawl and a beamtrawl. Differences in the catches between otter and beamtrawl are related with the higher catchability of swimmingand large-sized epibenthic species in the otter trawl, com-pared to the better sampling performance of beam trawlfor flat and slow fish and for sessile and small sized inverte-brates. Baca mesh size was of 60 mm in the net and 10 mmin the cod end. Horizontal opening was of 18.9 m and ver-tical opening of 2.0 m. The sampling unit was made up of30-min hauls during daytime at a speed of 3 knots. Beamtrawl horizontal opening was of 3.5 m and vertical openingof 0.6 m (mesh size of 10 mm). Beam trawls lasted 15 min ata mean speed of 2.5 knots. Both trawl gears were monitoredusing a Scanmar net control system. The mean area sweptwas 54728 ± 1532 m2 in otter trawls and 3307 ± 192 m2 inbeam trawls. Moreover, for each beam trawl the quantityof macroscopic heavy oil on the bottom was also obtained,which led the division of the Galician shelf into three zonesdepending on the amount of tar aggregates (Fig. 1): mini-mum impact (Zone 1), maximum impact (Zone 2) and med-

A. Serrano et al. / Marine Pollution Bulletin 53 (2006) 315–331 317

ium impact (Zone 3). Number of individuals and weight ofeach species were obtained from each Baca and beam trawl.

To study the suprabenthic fauna, a suprabenthic sledwas used, fitted with superposed nets of 3 m length and0.5 mm mesh size, which allowed quantitative samplingof the motile fauna in two water layers: 0–65 and 65–90 cm above the bottom. The sampling surface of the netswas 0.585 m2 in the lower net and 0.225 m2 in the upperone. Haul time was 2 min during daytime at a speed of 2knots. Sled trawl manoeuvres were also monitored usingScanmar system.

Infauna was collected using a modified Bouma box corer(0.0175 m2 surface area and 15–20 cm sediment depth). Fivesamples (0.0875 m2) were taken at each station in the depthstrata A and B. These samples were used for infaunal stud-ies and also for sediment analysis (grain size, organic mattercontent). Sieve size used in infaunal study was of 0.5 mm. Inthe deepest stratum (stratum C), only for the purposes ofsediment analysis (not represented in Fig. 1), a large boxcorer of 0.25 m2 sampling surface area was used. Particlesize analysis was performed by a combination of dry sievingand sedimentation techniques (Buchanan, 1984). Organicmatter content of the sediment, reported as % OM was esti-mated as weight loss of dried (100 �C, 24 h) samples aftercombustion (500 �C, 24 h). The main sedimentary charac-teristics were determined: percentage of organic matter,

Table 1Selected indicator or key species groups

Indicator group Scientific name(s)

Four-spot megrim Lepidorhombus boscii

Other flatfishes Arnoglossus laterna, A. imperialis, Microc

Dicologlossa cuneata, Solea solea, S. lasca

Forkbeard Phycis blennoides

Spotted dragonet Callyonimus maculatus

Triglidae Aspitrigla cuculus, Chelidonichthys gurnar

Chelidonichthys lucernus, Lepidotrigla cav

Pouting Trisopterus luscus

Catshark Scyliorhinus canicula

Monkfish Lophius piscatorius, Lophius budegassa

Rays Raja clavata, R. montagui, R. undulata, L

Pandalid shrimp Plesionika heterocarpus

Munida spp. M. sarsi, M. intermedia, M. iris

Megafaunal crabs Liocarcinus depurator, Macropipus tubercu

Paguridae Pagurus prideaux, P. excavatus, P. alatus,Norway lobster Nephrops norvegicus

Sea stars Astropecten irregularis, Marthastherias gla

Stichastrella rosea, Anseropoda placenta

Sea urchins Spatangus purpureus, Brissopsis lyrifera, E

Ophiuroidea AmphiuridaeMegafaunal Bivalvia Arcopagia balaustina, Astarte sulcata, Chl

Glycimeris glycimeris, Nucula sulcata, Spi

Venus casina, Venus verrucosa

Infaunal Bivalvia Abra spp., Thyasira spp.Polychaeta Ampharetidae, Capitellidae, SpionidaeSipunculida Golfingia vulgaris, Golfingia sp., Onchneso

Ampelisca sp. Ampelisca sp.Amphipoda AmphipodaCumacea CumaceaPeracarida Peracarida

Gear indicate belonging to the benthic compartments sampled with otter traw

mean particle diameter (Q50, in mm), sorting coefficient(S0), percentage of coarse sands (>500 lm), fine sands(62–500 lm) and mud (<62 lm).

2.2. Changes in ecological indices following the POS

To investigate the relationships among the environmen-tal variables (i.e., amount of tar aggregates, depth, latitude,organic matter, mean particle diameter, sorting coefficient,and weight percentage of coarse sand, fine sand and mud)and species richness, biomass and species diversity, thelevel of association of the three indices was examined usinga Spearman rank order correlation.

To analyse spatial variations among the three selectedzones, i.e., minimum impact, maximum impact and mediumimpact (spatial approach), differences in species richness(average species number per haul), biomass (average kgper haul), and Shannon–Wiener diversity (average diversityper haul) were examined using a one-way ANOVA on log-transformed data. When significant differences weredetected, we ran pairwise ‘‘a posteriori’’ Student–New-man–Keuls (SNK) test to identify the groups responsiblefor such differences. To study pre-spill and post-spillchanges for each selected area (temporal approach), differ-ences in species richness, biomass and species diversity werealso examined using a t-test.

Gear

OThirus variegatus, Buglossidium luteum,ris, Lepidorhombus whiffiagonis

OT, BT

OTOT, BT

dus, Chelidonichthys obscurus,illone, Trigla lyra

OT

OTOTOT

eucoraja naevus OTOT, BTOT, BT

latus, Goneplax rhomboides OT, BTP. bernhardus, Anapagurus laevis, A. petiti OT, BT

OT, BTcialis, Luidia sarsi, Luidia ciliaris, OT, BT

chinocardium cordatum, Echinus acutus OT, BTBC

amyx sp., Dosinia exoleta,sula elliptica, Venus striatula,

BT

BCBC

ma steenstrupii BCBC, SSBC, SSBC, SSBC, SS

l (OT), beam trawl (BT), box corer (BC) and suprabenthic sled (SS).

Fig. 2. Appearance of tar aggregates found in the grounds of the Galicianshelf in winter 2002. Photo: Francisco Sanchez.

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Fig. 3. Heavy oil (tar aggregates) average concentrations (kg km�2 ± SE)on the Galician continental shelf from five beam-trawl surveys.


2.3. Changes in indicator taxa densities following the POS

The taxa or groups of taxa selected as indicators (Table1) were based on previous works on oil sensitivity of epi-benthic fauna (Suchanek, 1993; Dean et al., 1996; Peterson,2001) and infaunal and suprabenthic fauna (Cabioch et al.,1980; Dauvin, 1982; Hyland et al., 1985; Spies, 1987; Jewettand Dean, 1997; Olsgard and Gray, 1995; Feder and Blan-chard, 1998).

For the analysis of epibenthic indicators, the historicalautumn series of otter trawl surveys (2001–2004) was takeninto account in order to get a better perspective (averagenumber of hauls = 51.5). Significant differences in meandensity (number of individuals per haul) among years weretested using a one-way ANOVA on log-transformed data.Relationships among environmental variables (includingamount of tar) and indicator densities were determinedusing a Spearman rank order correlation on log-trans-formed data. SIMPER analyses were run in order to iden-tify the main indicator taxa responsible for the majordissimilarities between the pre-POS and post-POS periods.

2.4. Effects of the POS and other environmental variables on

community structure

To assess the amount of variation in species biomass perhaul related to tar amount and a set of environmental vari-ables assumed to be important in community structure (i.e.,season, latitude, depth, percentage of organic matter, meanparticle diameter, sorting coefficient and weight percentageof coarse sands, fine sands and mud), a redundancy analy-sis (RDA) was used for otter trawl, beam trawl and box-corer analyses. Oil was recorded as weight of tar aggregatesper beam trawl sample. In addition, other sediment charac-teristics were recorded for each haul: organic matter con-tent, mean particle diameter, sorting coefficient andweight percentage of coarse sand, fine sand and mud ele-ments. RDA calculations were based on log-transformedabundance of all species collected. Species appearing in lessthan 5% of hauls were excluded. The statistical significanceof the first and all canonical axes together was tested by theMonte Carlo tests using 999 permutations under thereduced model. RDA results were presented graphicallyin a bi-dimensional ordination diagram generated by biplotscaling focusing on inter-species distances, in which sam-ples are represented by points and environmental variablesby vectors.

3. Results

3.1. Distribution of tar aggregates

As a result of the POS, the oil degradation and sedimen-tation through the water column caused the presence of taraggregates on the bottom. This heavy oil appeared inaggregates of between 1 and 20 cm in diameter (Fig. 2).The existence of particles of less than 10 mm could not

be determined owing to the beam trawl mesh size, whichmeans, with respect to the results obtained, that at leastthe quantities indicated were present. The concentrationsin each of the three zones considered, expressed inkg of oil km�2, are shown in Fig. 3. The highest mean con-centrations of oil were found in winter in Zone 2 (off Costada Morte), diminishing progressively over time until reach-ing very low levels (0.5 kg km�2) in October 2004, which isclose to our detection limit. In Zone 1, mean density of taraggregates was always very low (<0.1 kg km�2), and sothis study considers it to be the zone suffering the leastimpact.

Fig. 4 shows the spatial distribution of the tar aggregatesin four successive surveys, using geostatistical analysis (kri-

ging) to define contours of amounts. The greatest amountswere 300 kg km�2 in January 2003 at depths of 120–200 moff Cape Finisterre. According to the chemical fingerprintsof these samples (Albaiges pers. comm.), this oil has beenincorporated at the bottom after spending a short periodof time on the surface of the sea. This allows us to assumethat its distribution mainly follows that of an oil of greaterdensity, which sedimented in the first days following the

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Fig. 4. Tar aggregates spatial distribution in the study area sampled with beam-trawl. Density contours obtained using geostatistical analysis (kriging).


accident rather than degrading in the successive black tidesthat reached the coast. It is for this reason that the oil dis-tribution was found to coincide with the tanker�s drift dur-ing towing manoeuvres over the continental shelf beforesinking and also that tar aggregates were absent on theshelf of Zone 1, while the coast itself received considerableblack tides.

The presence of tar aggregates in January and April2003 shows a stable distribution pattern (Fig. 4), whichindicates little displacement by currents once sedimented.Lastly, the progressive fall in the concentrations of taraggregates on the continental shelf of Galicia is probably

due to their being covered by natural processes of sedimentaccumulation and because no new processes carrying oil tothe bottom have taken place. For this reason, concentra-tions are considerably reduced from spring, when great pri-mary production takes place in the area due to upwelling.

3.2. General faunal composition

The inventory of species obtained was 175 in theotter trawls, 277 in beam trawls, 159 in box corers and136 in suprabenthic sleds. Epibenthic dominant fauna inotter trawl samples were fishes (specially Micromesistius


poutassou, and with less importance, Scyliorhinus canicula

and Merluccius merluccius) followed by crustaceans, partic-ularly Plesionika heterocarpus. Epibenthic fauna sampledwith beam trawls was dominated by molluscs (with hugeabundances of Turritella communis), crustaceans (P. het-

erocarpus again showed the highest densities) and fishes(Arnoglossus laterna and Gadiculus argenteus as dominantspecies).

Polychaetes were the infaunal dominant group (thedominant species was the spionid polychaete Prionospio

fallax), followed by molluscs and crustaceans. Regardingthe suprabenthic compartment, a clear crustacean-domi-nated environment, mysids were the most abundant group(Leptomysis gracilis, Anchialina agilis, Boreomysismegalops, Erythrops neapolitana), followed by amphipods(Paramphilochoides odontonyx, Scopelocheirus hopei,Orchomenella nana), decapods (shrimps and crabs), cuma-ceans and isopods.

3.3. Changes in ecological indices following the POS

No significant correlations between tar aggregateamount and species richness, biomass, density and speciesdiversity (Table 2) were found, neither for epibenthicfauna (otter trawl and beam trawl), nor for infaunal (boxcorer) and suprabenthic (sled) communities. Significantcorrelations between other environmental variables andecological indices were detected, although most of themwith extremely weak values (Table 2). Depth shows a neg-ative correlation with biomass and species richness forbeam trawls and otter trawls, as well as a positive correla-tion with species diversity for box corers. Latitude also dis-plays a positive correlation with species richness anddensity for beam trawls and box corers. Among the sedi-ment characteristics, significant correlations were foundfor beam trawls, box corers and suprabenthic sled whichmay explain the relevance of the type of sediment to ben-thic communities.

Table 2Spearman rank order correlation (r) between environmental variables and spebeam trawl, otter trawl, box corer and suprabenthic sled

Beam trawl (n = 114) Otter trawl (n = 126

S W H 0 S W

Tar aggregates amount �0.083 0.049 �0.036 �0.020 0.141Depth �0.100 �0.460** 0.152 �0.288** �0.300**

Latitude 0.205* 0.010 0.171 0.156 0.108Organic matter (%) 0.049 �0.005 �0.047 0.094 0.080Mean particle diameter

(Q50)0.060 �0.236* 0.204* 0.006 �0.116

Sorting coefficient (S0) 0.104 0.105 �0.028 0.093 0.120Coarse sand (%) 0.157 0.110 0.061 0.137 0.117Fine sand (%) �0.059 �0.205* 0.184* �0.060 �0.079Mud (%) 0.026 0.196* �0.193* 0.026 0.065

* Significant correlations at p < 0.05.** Significant correlations at p < 0.001.

When changes in species richness, biomass and spe-cies diversity among zones of different impact (spatialapproach) for each survey were analysed, no significant dif-ferences were detected for beam trawls (Fig. 5). Neverthe-less, in the temporal approach, species richness anddiversity in the zone of maximum impact (Zone 2) were sig-nificantly higher (p < 0.05) in autumn 2003. Regardingspring surveys no differences were found.

In the sampling by otter trawl, an increase was detectedin species richness from Zone 1 to Zone 3 (p < 0.05) in thesurveys of spring 2004 and autumn 2004, although no sig-nificant differences were found in the other surveys (Fig. 6).We also detected an increase in biomass from Zone 1 toZone 3 in the winter immediately after the POS (p <0.05). All these results are more closely related to the lati-tude factor than to the impact by tar aggregates. Whenvariations between autumn surveys were examined, adecrease in species richness was detected in 2003 for allzones (Fig. 6), before recovering the following year. A sim-ilar pattern was found in species diversity.

3.4. Changes in indicator taxa densities after POS

Tar aggregate abundance did not show any significantcorrelation with indicator densities. Nevertheless, negativecorrelations between depth and Triglidae, Catshark andPaguridae densities were found (Table 3). Latitude andsediment characteristics represent important factors inexplaining box corer densities of infaunal indicators.

Focusing on the zone of maximum impact (Zone 2),among the indicator taxa or groups of taxa well-sampledin the otter trawls (rays and urchins did not present signif-icant yearly variations), all except pouting, monkfish andstarfishes showed a significant decrease in density in 2003with respect to pre-POS years (Fig. 7). All taxa exceptpouting and Paguridae presented a significant recoverythe following year with respect to 2003 (Fig. 7). Sea starsdisplay a significant increase in 2004 apparently unrelated

cies richness (S), biomass (W) or density (N) and species diversity (H 0) for

) Box corer (n = 16) Sled (n = 6)

H 0 S N H 0 S N H0

�0.151 0.358 0.107 0.118 0.034 0.068 �0.135�0.161 0.130 �0.366 0.583* 0.143 �0.771 0.028

0.167 0.730** 0.630* 0.265 0.143 �0.771 0.028�0.026 �0.525* �0.184 �0.294 0.677 �0.294 0.736

0.114 0.099 �0.230 0.617* 0.029 0.883* 0.029

�0.090 �0.026 0.288 �0.540* 0.029 0.883* 0.0290.096 0.342 0.376 0.041 �0.736 �0.647 �0.6770.086 0.076 �0.141 0.438 0.029 0.883* �0.029�0.108 �0.104 0.113 �0.465 0.029 �0.883* 0.029

Diversity (H')

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*

SPATIAL APPROACH TEMPORAL APPROACH

Fig. 5. Beam-trawl samples mean ecological indices (±SD) comparison from a spatial approach (between different impact level zones by season) and atemporal approach (between 2003 and 2004 years by zone and season). Labels represent season (W—winter, S—spring, A—autumn), year (02, 03, 04) andzone (1, 2, 3). An asterisk indicates a significant difference (p < 0.05).


to the POS. No significant changes along the historical ser-ies were found in the remaining taxa. Figs. 8–11 show thedecrease in 2003 and the recovery of 2004, and how theseshifts in indicators densities affected the whole area, notonly the maximum impact zone.

SIMPER multivariate analysis on the epibenthic indica-tors in the maximum impact zone indicated that the sametaxa that typified the post-POS decrease typified the clearrecovery in 2004 (Table 4). P. heterocarpus, Munida sp.and flatfishes were the three groups that most percentageof similarity explained in the perturbation dicotomy

(2002–2003), and also in the recovery dicotomy (2003–2004).

3.5. Effects of POS and other environmental variables on

community structure

Redundancy analysis (RDA) provided a bi-dimensionalordination of environmental variables, samples and spe-cies. The first three axes of beam-trawl RDA explained25.5% of species variation in the species per haul matrix,and 73.0% of variation in the ‘‘species–environment’’

Biomass (W)

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*


Fig. 6. Otter-trawl samples mean ecological indices (±SD) comparison from a spatial approach (between different impact level zones by season) and atemporal approach (between 2003 and 2004 years by zone and season). Labels represent season (W—winter, S—spring, A—autumn), year (02, 03, 04) andzone (1, 2, 3). An asterisk indicates a significant difference (p < 0.05). Bars under labels represent groups without significant differences.


matrix, 28.4% and 77.6%, respectively, being the varianceexplained in otter-trawl analysis. The Monte Carlo testsindicated that both the first axis (p = 0.002) and allcanonical axes together (p = 0.002) were significant in bothanalyses. Both beam-trawl (Fig. 12a) and otter-trawl(Fig. 12b) ordinations showed that depth is strongly corre-lated with Axis 1. Sediment typology was shown to be thesecond factor structuring epibenthos. In the beam-trawlRDA, the second axis was correlated with a sedimentgradient (Fig. 12a). Positive quadrants were related toheterogeneous and organic-enriched muddy sediments,while fine sands (poorer in organic matter) were associ-

ated with negative sectors. Axis 2 in the otter-trawl analysisalso displayed a high relationship with sediment typology,but more affected by particle diameter than by organicmatter content. Latitude showed a positive correlationwith poor fine sands in both analyses, and more relevantin the otter-trawl analysis. This correlation reflects the sed-imentary distribution in the area, with muddier sedimentsin the southern shelf. POS-related variables had a lowweight in the analyses. The maximum impact zone andtar aggregate density had low correlations with the axes.All POS-related variables discriminated in the positive seg-ment of Axis 2, related to muddy organic-enriched sedi-

Table 3Spearman rank order correlation between environmental variables andindicators densities for beam trawls, otter trawls and box corers

r

Beam trawl

Depth–Pagurids �0.700**

Otter trawl

Depth–Catshark �0.610**

Depth–Triglidae �0.710**

Box corer

Depth–Ampharetidae 0.760**

Depth–Cumacea 0.607*

Latitude–Peracarida 0.790**

Latitude–Amphipoda 0.770**

Latitude–Ampelisca sp. 0.603*

Latitude–Cumacea 0.740**

Coarse sand–Peracarida 0.620*

Coarse sand–Amphipoda 0.659**

Fine sand–Thyasira sp. �0.668**

Mud–Thyasira sp. 0.646**

r = correlation coefficient. (Only appear correlations with r > 0.60 andsignificant p value).

* Significant correlations at p < 0.05.** Significant correlations at p < 0.001.


ments. Likewise, seasonal variables also made a low contri-bution to axes building, showing low discriminatory power.

The discrimination of samples is shown in Fig. 12c andd. In both analyses, plots separated samples following adepth criterium. Beam-trawl analysis (Fig. 12c) shows threewell-defined groups: a 70–120 m coastal group (with thediscrimination of a subgroup of muddier samples), 121–200 m inner shelf group and a 201–300 middle and outer-shelf group. Inter-sample variability was higher in thecoastal group than in deeper groups. The same patterncan also be observed in the otter-trawl RDA plot, but witha lower discrimination due to the lesser importance of sed-imentary factors.

RDA ordination of the infaunal box corer matrix oncemore showed a dominance of depth over other variables(Fig. 13). Paradoxically, sedimentary variables seem to beof less importance in the building of Axis 2 with respectto epibenthic beam and otter trawls. This fact is attribut-able to the lower N (16 box-corer samples vs 114 beamtrawl and 126 otter trawl). Latitude and Zone 2, dominantvariables in Axis 2, may suggest a POS effect in infaunalcommunities. Although this hypothesis cannot be rejected,it is obvious that these variables also reflect a sedimentarygradient, splitting the southern muddier samples of Zone 1.Problems with the box corers at great depths prevented thesampling of the 201–300 stratum, the muddier stratum inZone 2, in contrast with beam and otter trawls in whichmuddy sediments are represented in all zones. Box-corersamples were located following depth-zone criteria(Fig. 13).

In conclusion, the RDA�s did not provide evidence ofany patterns of similarity among samples attributable tocontamination by tar aggregates. The low importance of

tar aggregate abundance and the maximum impact zonealso indicate that no indicator species or groups of specieshave shown remarkable impact effects. Depth, therefore,and to a lesser extent sediment particle diameter, stronglyinfluence epibenthic communities. Organic matter contentin the sediment is a third key variable in smaller-sizedepibenthic (beam trawl), infaunal and suprabenthic com-munities, but not in larger epibenthic communities (ottertrawl).

4. Discussion

The results obtained in the present work suggest thattar aggregates found on the bottoms of the Galician conti-nental shelf after the Prestige oil spill did not affect thedistribution of benthic communities. Spatial patterns inshelf assemblages are strongly influenced by natural physi-cal conditions rather than POS toxicity, which is consis-tent with the results of Guidetti et al. (2000). The lowbioavailability of Prestige tar aggregates probably providesthe explanation for these results. In other spills, physicalfactors determining oil availability were stated as an impor-tant factor. For example, the formation of the neutrallybuoyant oil–clay flocculates within the Exxon Valdez

oil spill slick and the major currents within Prince WilliamSound were apparently important in preventing substan-tial oil accumulation at depth (Feder and Blanchard,1998). Other works found hydrocarbon concentrations inbottom sediments after the oil spill but no significant effectson benthic fauna at depths greater than 40 m (Braer oilspill: Kingston et al., 1995; Exxon Valdez oil spill:Armstrong et al., 1995; Feder and Blanchard, 1998). Incontrast, in a study on the Exxon Valdez oil spill atdepths less than 20 m, oil hydrocarbon concentrationsexplained significant proportions of the variation in ben-thic community structure between oiled and unoiled sites(Jewett et al., 1999). Sanders et al. (1980) also conclude thatpatterns of disturbance at depths less than 10 m wererelated to high concentrations of oil, rather than granulom-etry. Apparently oil effects tend to diminish with increasingdepth.

The main environmental variables explaining the spatialdistribution of Galician shelf epibenthic communities, bothotter and beam trawls, are depth and type of sediment.These variables constitute the main structuring factors overseasonal or spill-related variables. Epibenthos sampledwith beam trawl are more affected by sediment typologythan the fauna collected with otter trawl. These environ-ment–species relationships have already been described(Olaso, 1990; Sanchez and Serrano, 2003; Serrano et al.,in press) for the Cantabrian continental shelf.

Regarding the infaunal and suprabenthic communities,the amount of tar aggregates did not determine communitydistribution, either. As in epibenthic compartment, ecolog-ical indices were correlated with depth and sediment typol-ogy. The importance of the ‘‘latitude’’ factor on infaunaland suprabenthic communities reflects the sedimentary

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Crabs Paguridae

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--- ------ ---Fig. 7. Densities (number/30 min otter trawl ±SE) of indicator species or groups of species in the pre-POS and post-POS periods.


distribution of the Galician shelf, with muddier sedimentsin the southern shelf related to the upwelling and outwel-ling processes of the Rıas Baixas estuarine systems(Lopez-Jamar et al., 1992). These results match those ofFeder and Blanchard (1998), in which no detectableresponse was found in subtidal infauna following theExxon Valdez spill.

The lack of correlations between the distribution ofmacroscopic tar aggregates and the distribution of allbenthic compartments does not imply an absence ofeffects of the POS in shelf communities. Soluble compo-nents and toxic sea snow (microparticled oil, oiled plank-ton) are not estimated by our methodology, and thesesources of toxicity may affect the whole area. Once the

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FLATFISHESDensity (no/haul)

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Autumn 2002


Autumn 2003


Autumn 2004

Fig. 8. Spatial distribution of flatfishes (L. boscii excluded) densities in the study area in the pre-POS and post-POS periods (historical series of otter trawlsurveys 2001–2004).


oil or its derivatives reach the sediment, there exists awhole series of physico-chemical processes which willdetermine its bioavailability (Peterson, 2001). The pro-cesses of bioaccumulation are negatively correlated withoil particle size, and those processes will be greater indetritivorous benthic organisms than in suspension feed-ers and will be modulated by the duration of their lifecycle, detoxification capacity and lipid content (liposolu-ble xenobiotic compounds). The ingestion of hydrocar-bons in these organisms, PAHs in particular, may notcause lethal effects (if the dose is not high) but will leadto genetic, biochemical and physiological changes that

may reduce their viability and biological efficiency, andfinally to the decline of their populations (Peterson,2001).

The fall in the indicator densities in 2003 may reflectbottom-up changes derived from the POS, although thesechanges may also be related to other factors not taken intoaccount in this work. Factors such as upwelling and out-welling processes are of great importance to the benthicregime of the Galician shelf (Lopez-Jamar et al., 1992),determining primary and secondary production changes.Furthermore, Prestige oil slicks were driven alongthe northern Spanish coast by the ‘‘Navidad’’ flow, an

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FORKBEARD

Density (no/haul)

Autumn 2001

FORKBEARD

Density (no/haul)

Autumn 2002

FORKBEARD

Density (no/haul)

Autumn 2003

FORKBEARD

Density (no/haul)

Autumn 2004

Fig. 9. Spatial distribution of forkbeard (Phycis blennoides) densities in the study area in the pre-POS and post-POS periods (historical series of otter trawlsurveys 2001–2004).


important hydrographic agent that affects the recruitmentof several species (Sanchez et al., 2003a,b). Moreover, Nav-idad flow presented its fourth strongest development overthe last 25 years in the winter of 2002 (Garcıa-Soto,2004). It is therefore possible that the strength of thedevelopment of this winter hydrographic structure in2002 might influence benthic communities by larval advec-tion or other transport mechanisms, reflecting in recruit-ment failure and, finally, decreases in density in autumn2003.

Epibenthic indicators showing a clear decrease in 2003were species with a higher muddy-affinity, and benthopha-gous fishes (Preciado et al., 2002). The decline of Norway

lobster (Nephrops norvegicus) density is consistent withthe decrease in the relative importance of landings of thisspecies in the hake-megrim-monk-Nephrops fleet compo-nent (Punzon et al., 2005). Norway lobster is a specieswith a burrowing behaviour, and so its decrease may berelated to contaminated sediments (Sanchez et al., thisvolume).

The rapid recovery of indicator taxa in autumn 2004 isremarkable. Several studies reported benthic long-termrecovery over 3–15 years following oil spills (e.g. Parraand Lopez-Jamar, 1997). In contrast, there are scarcereports on the quick rebound of benthic fauna after post-spill decreases (Elmgren et al., 1983; Driskell et al., 1996).

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DRAGONET

Density (no/haul)

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DRAGONET

Density (no/haul)

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SPOTTED

DRAGONET

Density (no/haul)

Autumn 2003

SPOTTED

DRAGONET

Density (no/haul)

Autumn 2004

Fig. 10. Spatial distribution of spotted dragonet (Callyonimus maculatus) densities in the study area in the pre-POS and post-POS periods (historical seriesof otter trawl surveys 2001–2004).


Dean et al. (1996) explained the recovery of helmet crabdensities after the Exxon Valdez oil spill by emigrationfrom unoiled adjacent sites. Nevertheless, the absence ofunoiled areas in the shelf after the POS and the evidenceof density decreases throughout the Galician shelf mayindicate that the origin of recovery is to be found in causesother than emigration. Enhanced nutrient availability andchanges in interspecific relationships, such as a decreasein predation or competition pressure, may be causes ofthe rebound effect detected.

The decline in sensitive taxa at shallow depths in theExxon Valdez oil spill had little impact on higher trophiclevels (Dean et al., 1996). Likewise, Punzon et al. (2005)

did not find significant changes on feeding habits of themain commercial fish species. On the other hand, no evi-dence was found of top-down effects derived from the clo-sure of fishing activities, since the most noteworthy changesaffected lower trophic levels and benthophagous fishes, nottop predator commercial species.

Unlike epibenthic indicators, changes in infaunal indica-tor densities were not found, neither for opportunistic spe-cies nor for sensitive ones, although data from the samestations prior to the spill are not available. The oppositeoccurred following the Aegean Sea spill, which was morecoastal and more highly concentrated spatially than thePOS. Noteworthy effects on the Galician coastal infaunal

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10.0˚ 9.5˚ 9.0˚ 8.5˚ 8.0˚

42.5˚

43.0˚

43.5˚

44.0˚

0

50

100

200

400

10.0˚ 9.5˚ 9.0˚ 8.5˚ 8.0˚

42.5˚

43.0˚

43.5˚

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0

50

100

200

400

10.0˚ 9.5˚ 9.0˚ 8.5˚ 8.0˚

42.5˚

43.0˚

43.5˚

44.0˚

0

50

100

200

400

10.0˚ 9.5˚ 9.0˚ 8.5˚ 8.0˚

42.5˚

43.0˚

43.5˚

44.0˚

0

50

100

200

400

CRABSDensity (no/haul)

Autumn 2001


Autumn 2002


Autumn 2003


Autumn 2004

Fig. 11. Spatial distribution of crab densities in the study area in the pre-POS and post-POS periods (historical series of otter trawl surveys 2001–2004).

Table 4Otter trawl epibenthic indicators taxa explaining 50% of dissimilarity between 2002 and 2003 (perturbation), and between 2003 and 2004 (recovery), forthe maximum impact zone (Zone 2)

2002 vs 2003, d = 54.15 N 2002 N 2003 di (%) 2003 vs 2004, d = 53.99 N 2003 N 2004 di (%)

Plesionika heterocarpus 1697.50 67.63 14.54 Plesionika heterocarpus 67.63 3750.00 11.87Munida sp. 177.79 31.00 24.56 Munida sp. 31.00 866.53 20.61Flatfishes 129.86 35.44 32.55 Flatfishes 35.44 223.47 27.75Four-spot megrim 70.07 22.63 38.13 Crabs 0.63 33.73 34.35Forkbeard 6.93 1.19 43.72 Spotted dragonet 1.25 12.00 39.95Spotted dragonet 4.43 1.25 48.03 Four-spot megrim 22.63 77.60 44.60Crabs 7.43 0.63 51.53 Sea stars 3.94 11.60 49.09

Triglidae 1.00 5.60 53.12

N = number/haul in each group; d = average dissimilarity; di (%) = cumulative dissimilarity of indicator i.


a b

c d

Fig. 12. RDA ordination plots of (a) environmental variables in beam-trawl samples; (b) environmental variables in otter-trawl samples; (c) beam-trawlsamples; (d) otter-trawl samples. Sample labels represent season (winter: w, spring: s, autumn: a), year (2002: 2; 2003: 3; 2004: 4) and depth strata (70–120 m: A; 121–200 m: B; 201–300 m: C).


communities were detected, specifically enhanced densitiesof opportunistic polychaeta (Parra and Lopez-Jamar,1997) and the disappearance or drastic reduction of sensi-tive amphipoda (Gomez Gesteira and Dauvin, 2000; Parraand Lopez-Jamar, 1997).

Nevertheless, a historical perspective is required tocorroborate the epibenthic indicator decrease/reboundshifts of 2002–2003 or the absence of infaunal indicatorchanges, since important interannual fluctuations in ben-thic fauna may be characteristic in the Galician continentalshelf.

All these facts emphasize the need for continuousand holistic monitoring of oil spills. Following thatperspective, this study was carried out in the framework

of a multidisciplinary project, which enabled its results tobe contrasted with those of parallel studies focusing onthe effects on commercial species and their feeding habits(Sanchez et al., this volume), effects on fishing activi-ties (Punzon et al., 2005) or biological effects on fish(Martınez-Gomez et al., this volume). Finally, all thisecosystem information will be pooled together in a massbalance model of trophic interactions (Ecopath, withdynamic routines Ecosim and Ecospace) with the aim ofdetecting long-term effects of the POS, or in other words,to know whether shifts in abundances will ever result insubsequent cascading effects on the trophic web. Only withthis understanding will we have the tools to protect andconserve such diverse natural resources.

-1.0

-1.0

1.0

1.0

Zone 2

Spring

WinterTar

Latitude

Depth

O.M.

Q50

So

Coarse sands

Fine sands

Mud w1A

s1A

w1B

s1B

w1A

s1A

w1Bs1B

w2B

s2B

w2As2A

w2B

s2B

w2Bs2B

-1.0

-1.0

1.0

1.0

-

-1.0

1.0

1.0

-1.0

1.0

1.0

e

o

w1A

s1A

w1B

s1Bs1A

Fig. 13. RDA ordination biplot of environmental variables and samplesin infaunal box-corer analysis. Sample labels represent season (winter: w,spring: s, autumn: a), zone (1, 2, 3) and depth strata (70–120 m: A; 121–200 m: B).


Acknowledgements

This study was made possible thanks to the invaluablework of all the participants in the North of Spain bot-tom trawl surveys and the crews of the two research vesselsCornide de Saavedra and Vizconde de Eza. The commentsof the referee S.C. Jewett are greatly appreciated, helpingto improve the impact of this paper. We are grateful toDr. Joan Cartes and to Emanuella Fanelli of the I.C.M.(Barcelona) for their fruitful collaboration. This studywas partially supported by the Urgent and StrategicActions of the Spanish Science and Technology Ministry,and included in the ECOPREST Project (VEM2003-20081-CO2).

References

Armstrong, D.A., Dinnel, P.A., Orensanz, J.M., Armstrong, J.L.,Mcdonald, T.L., Cusimano, R.F., Nemeth, R.S., Landolt, M.L.,Skalsi, J.R., Lee, R.F., Huggett, R.J., 1995. Status of selected bottomfish and crustacean species in Prince William Sound following theExxon Valdez oil spill. In: Wells, P.G., Butler, J.N., Hughes, J.S.(Eds.), Exxon Valdez Oil Spill: Fate and Effects in Alaskan Waters.Amer. Soc. Testing & Materials, Philadelphia, PA, USA, pp. 485–547.

Bode, A., Alvarez-Ossorio, M., Gonzalez, N., Varela, M., Varela, M.M.,2003. Informe preliminar sobre el muestreo del radial de A Coruna endiciembre de 2002 y enero de 2003. IEO Prestige web Report, no. 8., 11pp. Available from: <www.ieo.es/prestige/informe08.htm>.

Buchanan, J.B., 1984. Sediment analysis. In: Holme, N.A., McIntyre,A.D. (Eds.), Methods for the Study of Marine Benthos. BlackwellScientific Publications, Oxford, pp. 41–65.

Cabioch, L., Dauvin, J.C., Mora Bermudez, J., Rodrıguez Babio, C.,1980. Effects de la maree noire de l�Amoco Cadiz sur le benthos

sublittoral du nord de la Bretagne. Helgol. Wiss. Meeresunters 33,192–208.

Dauvin, J.C., 1982. Impact of Amoco Cadiz oil spill on the muddy finesand Abra alba and Melinna palmata community from the Bay ofMorlaix. Estuar. Coast. Shelf Sci. 14, 517–532.

Dean, T.A., Jewett, S.C., Laur, D.R., Smith, R.O., 1996. Injury toepibenthic invertebrates resulting from the Exxon Valdez oil spill. In:Spies, R.B., Wolfe, D.A., Wright, B.A. (Eds.), Proceedings of theExxon Valdez Symposium. American Fisheries Society Symposium,pp. 424–439.

Driskell, W.B., Fukuyama, A.K., Houghton, J.P., Lees, D.C., Mearns,A.J., Shigenaka, G., 1996. Recovery of Prince William Soundintertidal infauna from Exxon Valdez oiling and shoreline treatments,1989 through 1992. In: Spies, R.B., Wolfe, D.A., Wright, B.A. (Eds.),Proceedings of the Exxon Valdez Symposium. American FisheriesSociety Symposium, pp. 362–378.

Elmgren, R., Hansson, S., Larsson, U., Sundelin, B., Boehm, P.D., 1983.The Tsesis oil spill: acute and long-term impact on benthos. Mar. Biol.73, 51–65.

Feder, H.M., Blanchard, A., 1998. The deep benthos of Prince WilliamSound, Alaska, 16 months after Exxon Valdez oil spill. Mar. Poll. Bull.36, 118–130.

Frutos, I., Parra, S., 2004. Primeros resultados sobre el efecto del vertidodel petrolero Prestige sobre las comunidades suprabentonicas de laplataforma continental proxima a la Rıa de La Coruna (NW,Penınsula Iberica). XIII Simposio Iberico de Estudios del BentosMarino (Las Palmas 21–24 septiembre, 2004).

Garcıa-Soto, C., 2004. Prestige oil spill and Navidad flow. J. Mar. Biol.Assoc. UK 84, 297–300.

Gomez Gesteira, J.L., Dauvin, J.-C., 2000. Amphipods are good bioin-dicators of the impact of oil spills on soft-bottom macrobenthiccommunities. Mar. Poll. Bull. 40, 1017–1027.

Guidetti, P., Modena, M., La Mesa, G., Vacchi, M., 2000. Composition,abundance and stratification of macrobenthos in the marine areaimpacted by tar aggregates derived from the Haven oil spill (LigurianSea, Italy). Mar. Poll. Bull. 40, 1161–1166.

Hyland, J.L., Hoffman, E.J., Phelps, D.K., 1985. Differential responses oftwo nearshore infaunal assemblages to experimental petroleum addi-tions. J. Mar. Res. 43, 365–394.

Jewett, S.C., Dean, T.A., 1997. The effects of the Exxon Valdez oil spill oneelgrass communities in Prince William Sound, Alaska 1990–95.Restoration Project 95106. Final Report to Exxon Valdez Oil SpillTrustee Council, Anchorage.

Jewett, S.C., Dean, T.A., Smith, R.O., Blanchard, A., 1999. Exxon Valdez

oil spill: impacts and recovery in the soft-bottom benthic community inand adjacent to eelgrass beds. Mar. Ecol. Prog. Ser. 185, 59–83.

Kingston, P.F., Dixon, I.M.T., Hamilton, S., Moore, D.C., 1995. Theimpact of the Braer oil spill on the macrobenthic infauna of thesediments off the Shetland Islands. Mar. Poll. Bull. 30, 445–459.

Lopez-Jamar, E., Cal, R.M., Gonzalez, G., Hanson, R.B., Rey, J.,Santiago, G., Tenore, K.R., 1992. Upwelling and outwelling effects onthe benthic regime of the continental shelf off Galicia, NW Spain. J.Mar. Res. 50, 465–488.

Martınez-Gomez, C., Campillo, J.A., Benedicto, J., Fernandez, B., Valdes,J., Garcıa, I., Sanchez, F., this volume. An assessment of the biologicaleffects related to the Prestige oil spill applying biomarkers in demersalfish (Lepidorhombus boscii and Callionymus lyra) from the northernIberian shelf. Mar. Poll. Bull.

Olaso, I., 1990. Distribucion y abundancia del megabentos invertebradoen fondos de la plataforma cantabrica. Publ. Esp. Inst. Esp. Oceanogr.5, 1–128.

Olsgard, F., Gray, J.S., 1995. A comprehensive analysis of the effects ofoffshore oil and gas exploration and production on the benthiccommunities of the Norwegian continental shelf. Mar. Ecol. Prog. Ser.122, 277–306.

Parra, S., Lopez-Jamar, E., 1997. Cambios en el ciclo temporal de algunasespecies endofaunales como consecuencia del vertido del petroleroAegean Sea. Publ. Esp. Ins. Esp. Oceanogr. 23, 71–82.

http://www.ieo.es/prestige/informe08.htm


Pearson, T.H., Rosenberg, R., 1978. Macrobenthic succession in relationto organic enrichment and pollution of the marine environment.Oceanogr. Mar. Biol. Ann. Rev. 16, 229–311.

Peterson, C.H., 2001. The Exxon Valdez oil spill in Alaska: acute, indirectand chronic effects on the ecosystem. Adv. Mar. Biol. 39, 1–103.

Peterson, C.H., Rice, S.D., Short, J.W., Esler, D., Bodkin, J.L., Ballachey,B.E., Irons, D.B., 2003. Long-term ecosystem response to the Exxon

Valdez oil spill. Science 302, 2082–2086.Preciado, I., Gutierrez-Zabala, J.L., Velasco, F., Olaso, I., 2002. Dieta de

otono de once especies de peces demersales en la plataforma atlanticadel sur de Galicia. Nova Acta Cient. Comp. 12, 125–141.

Punzon, A., Hernandez, C., Abad, E., Trujillo, V., Castro, J., 2005.Possible changes on exploitation strategies of the most importantfisheries due to the Prestige oil spill. Symposium on Marine AccidentalOil Spills (VERTIMAR), Vigo (Spain), July 2005, 146–147.

Sanchez, F., 2003. Presencia y cuantificacion del fuel sedimentado en lasplataformas de Galicia y mar Cantabrico. IEO Prestige web report no.14, 7 pp. Available from: <www.ieo.es/prestige/informe14.htm>.

Sanchez, F., Blanco, M., Gancedo, R., 2002. Atlas de los peces demersalesy de los invertebrados de interes comercial de Galicia y el Cantabrico.Otono 1997–1999. Ed. CYAN (Inst. Esp. Oceanogr.).

Sanchez, R., Sanchez, F., Gil, J., 2003a. The optimal environmentalwindow that controls hake (Merluccius merluccius) recruitment in theCantabrian Sea. ICES Mar. Sci. Symp. 219, 415–417.

Sanchez, R., Sanchez, F., Landa, J., Fernandez, A., 2003b. Influence ofoceanographic parameters on recruitment of megrim (Lepidorhombus

whiffiagonis) and four-spot megrim (L. boscii) on the Northern Spanish

continental shelf (ICES Division VIIIc). ICES Mar. Sci. Symp. 219,400–402.

Sanchez, F., Serrano, A., 2003. Variability of groundfish communities ofthe Cantabrian Sea during the 1990s. ICES Mar. Sci. Symp. 219, 249–260.

Sanchez, F., Velasco, F., Cartes, J.E., Olaso, I., Preciado, I., Fanelli, E.,Serrano, A., Gutierrez-Zabala, J.L., this volume. Monitoring thePrestige oil spill impacts on some key species of the northern Iberianshelf. Mar. Poll. Bull.

Sanders, H.L., Grassle, J.F., Hampson, G.R., Morse, L.S., Garner-Price,S., Jones, C.C., 1980. Anatomy of an oil spill: long-term effects fromthe grounding of the barge Florida off West Fallmouth, MA. J. Mar.Res. 38 (2), 265–280.

Serrano, A., Sanchez, F., Garcıa-Castrillo, G., in press. Epibenthiccommunities of trawlable grounds of the Cantabrian Sea. Sci. Mar.

Spies, R.B., 1987. The biological effects of petroleum hydrocarbons in thesea: assessments from the field and microcosms. In: Boesch, D.F.,Rabalais, N.N. (Eds.), Long-Term Environmental Effects of OffshoreOil and Gas Development. Elsevier Applied Science, pp. 411–467.

Sturdevant, M.V., Wertheimer, A.C., Lum, J.L., 1996. Diets of juvenilepink and chum salmon in oiled and non-oiled nearshore habitats inPrince William Sound, 1989 and 1990. In: Spies, R.B., Wolfe, D.A.,Wright, B.A. (Eds.), Proceedings of the Exxon Valdez Symposium.American Fisheries Society Symposium, pp. 578–592.

Suchanek, T.H., 1993. Oil impacts on marine invertebrate populations andcommunities. Amer. Zool. 33, 510–523.

http://www.ieo.es/prestige/informe14.htm

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Spatial and temporal changes in benthic communities of the Galician continental shelf after the Prestige oil spill