Variations in benthic fauna underneath an effluent mixing zone

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Variations in benthic fauna underneath an effluent mixing zoneat a marine oil terminal in Port Valdez,AlaskaArny L.Blanchard *,Howard M.Feder,David G.ShawInstitute of Marine Science,School of Fisheries,Ocean Sciences,University of Alaska,P.O.Box 757220,Fairbanks,Alaska 99775-7220,USAAbstractThe distributions of hydrocarbons and infauna in sediments below a permitted mixing zone for the disposal of treated ballast waters in Port Valdez,Alaska were examined annually,1999–2001.The associations of biological measures and the abundance of selected benthic organisms to total aromatic hydrocarbons (TARO)ranged up to large-sized effects,as compared against minimum-effect criteria (j r j P 0:63).The apparent sensitivity of three polychaete worms to low levels of hydrocarbons makes them particularly useful as indicators of future changes in spatial distributions of hydrocarbons associated with discharged effluent.In 2001,sediment TARO concentrations decreased and the correlation values of TARO to biotic variables were generally less than in 1999and 2000.Evidence supports a conclusion of a strong but spatially limited association of some fauna with accumulations of petroleum hy-drocarbons in these sediments.Ó2003Elsevier Ltd.All rights reserved.Keywords:Port Valdez,Alaska;Hydrocarbons;Disturbance;Infauna;Galathowenia ;Melinna ;Axinopsida1.IntroductionPort Valdez,a fjord within Prince William Sound,Alaska,is the terminus of the Trans-Alaska oil pipeline (Fig.1).Interest in protecting this fjord from environ-mental damage by human activities is high and concerns include the disposal of treated ballast waters from in-coming tankers at a marine oil terminal (Blanchard et al.,2002).Oily ballast water is offloaded from arriving tankers and transferred to an onshore treatment plant before crude oil can be loaded.Ballast water is treated to remove crude oil and then discharged through an outfall line fitted with diffuser ports (the diffuser)some 50m from shore in depths of 65–75m (see Shaw and Hameedi,1988;Blanchard et al.,2002for details on quantities,sources,and fate of hydrocarbons in Port Valdez).Alteration of infaunal communities in marine envi-ronments receiving petroleum residues has been ob-served.Pearson and Rosenberg (1978)demonstrate that tolerant species can occur close to a source of pollutants,grading to intolerant organisms a distance away.Fieldstudies of the effects of oil and gas exploration on ben-thic infauna (considering both drilling mud and associ-ated hydrocarbon burdens)show such trends (e.g.,Gray et al.,1990;Olsgard and Gray,1995;Montagna and Harper,1996).Similar patterns also occur at natural marine oil seeps where infauna assemblages exhibit lower diversity and dominance by opportunistic organ-isms (Spies and Davis,1979;Steichen et al.,1996).En-richment of faunal communities (increased densities of some taxa within the ambient benthic assemblage due to locally increased food resources from allochthonous sources)also can occur over short distances due to in-creased numbers of bacteria associated with the degra-dation of oil (Spies and Davis,1979).Likewise,investigations near marine oil terminal facilities show increased abundances of opportunistic polychaetes (capitellid,cirratulid,and spionid polychaetes)in asso-ciation with increased sediment hydrocarbons (Seng et al.,1987;Westwood et al.,1987;May and Pearson,1995;Blanchard et al.,2002).Following a short-term,localized contamination of sediments by weathered hy-drocarbons and an increase in opportunistic taxa at a site close to the diffuser in Port Valdez (Blanchard et al.,2002),we initiated a study in 1998to assess spatial and temporal aspects of sediment hydrocarbon distributions below the permitted mixing zone (Shaw et al.,1999).*Corresponding author.E-mail addresses:arnyb@ (A.L.Blanchard),feder@ (H.M.Feder),ffdgs@ (D.G.Shaw).0025-326X/$-see front matter Ó2003Elsevier Ltd.All rights reserved.doi:10.1016/S0025-326X(03)00324-2/locate/marpolbulMarine Pollution Bulletin 46(2003)1583–1589Selected sites were re-sampled annually,1999through 2001,and biological sampling was included.The con-clusions from the study are discussed here.2.MethodsThe sampling transect lies on the main axis of a hy-drocarbon gradient adjacent to the diffuser(Shaw et al., 1999).These sampling locations,Stations141–147(es-tablished in1998),211(established in1999),203and204 (established in2000,positioned to follow the depth contour and to avoid physical obstructions),and212 (established in2000)(Fig.1),are62–85m deep.Data from single biological samples archived from the1998 investigation(Stations142,143,and146)are presented in tables andfigures but not used in correlation analyses. Samples were collected in the last week of August orfirst week of September using a van Veen grab(0.1m2). Hydrocarbon and biological samples were collected from each grab and analyzed according to methods outlined in Blanchard et al.(2002).Hydrocarbon results are summarized as the sum of18individually quantified aromatics(total aromatics(TARO)).Biological mea-sures include infaunal abundance,biomass,and number of taxa as well as the abundance of11numerically dominant taxon groups.Correlation values were determined between TARO and selected biotic variables including total abundance, biomass,number of taxa,and the abundance of selected taxon groups for each year.The natural logarithmic transformation was applied to TARO values.Numeri-cally dominant taxa were selected for correlation ana-lysis.Correlation values were determined using data for individual samples rather than station means.In an application of the minimum-effects hypothesis(Murphy and Myors,1998),Blanchard et al.(2002)suggested standardized effect sizes(Cohen,1988)for invertebrate studies of small,f¼0:2;medium,f¼0:5;and large, f¼0:8.These effect-size criteria are converted to crite-ria appropriate for correlation testing(Cohen,1988), with coefficients of j r j P0:2considered small effects, coefficients of j r j P0:45considered medium effects,and coefficients of j r j P0:63considered as large effects. Correlation coefficients less than0.2are considered negligible.Relative to1999and2000,2001substrates were very compact and exceptionally difficult to sample. Grabs were often less than full,so rank correlation methods were used for2001.3.ResultsAverage TARO,and abundance and biomass of in-fauna are presented in Table1.TARO concentration and infaunal density were highest at Station143in1998 reaching values of755.1ng gÀ1and2760ind.mÀ2,re-spectively.Biomass was highest,8.3g mÀ2,at Station 146in2000,and the‘‘number of taxa’’greatest at Sta-tion142in2000,with31taxa observed.The lowest TARO concentration,11.8ng gÀ1,was observed at Station211in1999,while the lowest faunal density, biomass,and number of taxa,150ind.mÀ2,0.9g mÀ2, and11taxa,were observed at Station141in2000.The high average abundance at Station143in1998reflects high densities of the polychaetes Capitellidae(520in-d.mÀ2;dominated by worms in the genus Capitella), Cirratulidae(720ind.mÀ2),and Polydora socialis(290 ind.mÀ2)and the thyasirid bivalve Axinopsida serricata (920ind.mÀ2)(Table2and Fig.2).Capitellid and cirratulid worms were less abundant in other years.Correlation analyses indicate some medium and large associations between TARO and biotic variables.The relationship of TARO to total abundance and biomass for1999shows medium-sized effects(j r j P0:45;Table 3).For2000,the association of TARO to abundance is medium-sized while the association of the number of taxa to TARO is large(j r j P0:63).For2001,the rank associations of abundance and biomass to TARO are small(j r j P0:20)but large for the number of taxa.The abundance values of A.cyclia,A.serricata,and P.so-cialis for1999and2000,are positively correlated to TARO with generally medium to large-sized effects (Table3).All these taxa demonstrated peaks in abun-dance near the diffuser(Fig.2).Mostly large,negative (inverse)associations are observed between the abun-dance values of Melinna cristata,Galathowenia oculata, and Nephtys punctata and TARO in1999and2000.The numbers of these organisms,and particularly those of M.cristata,are reduced close to the diffuser.However, neither G.oculata or M.cristata are particularly abun-dant at any of the sampling locations.The abundance values of polychaete taxa Cirratulidae,Capitellidae, Exogone spp.,and P.steenstrupi are not clearlyrelatedto TARO as correlation values were small or negligible (Table3).In2001,rank correlation values are of a smaller size as only two values between taxon groups and TARO,for G.oculata and Lumbrineris sp.,are medium-sized.All others are small or negligible.4.DiscussionLong-term,broad-scale studies in Port Valdez(Feder et al.,1973;Feder and Matheke,1980;Feder and Jewett, 1988;Blanchard et al.,2002)were designed to provide a record for subtidal infaunal communities against which disturbance due to increased sediment hydrocarbons could be identified.Pearson and Rosenberg(1978)sug-gest that disturbance due to organic enrichment will be apparent as a rise in the numbers of opportunists fol-lowed by decreases in sensitive taxa with increasing pollution.Blanchard et al.(2002)indicate that this is the pattern likely to be observed in Port Valdez because of the lack of sensitive taxa(e.g.,echinoderms and am-phipods)in the study area and treatment of the ballast waters.In1995–1997a rise in opportunists followed by a decrease in all taxons was observed at one station in Port Valdez in association with sediment contamination near the diffuser(Blanchard et al.,2002).The spacing of sampling locations in that study,however,was broader than the range of effects and did not allow for the identification of chronic effects.Following this distur-bance event in1995–1997,the present study was initi-ated on a smaller-scale to document temporal changes in the distribution and concentrations of hydrocarbons derived from diffuser effluent in sediments as well as any associated biological effects.Correlations noted in this study indicate a strong association between the benthic community in Port Valdez and hydrocarbons from diffuser effluents.Rela-tionships between TARO and biotic measures are mostly of lesser magnitude but occasionally large(as determined by comparison against minimum-effect cri-teria).Medium to large correlations are recorded for the abundances of numerically dominant taxa,suggesting a moderate but mixed influence(i.e.,both positive and negative associations)of hydrocarbon concentrations on biota.In2001,the TARO concentrations were lower and strength of correlations decreased.These associations doTable1Average total aromatics(TARO),percent total organic carbon(TOC)abundance,and biomass for the grid stations sampled in1998and1999 (values for stations with multiple replicates are averages)Year Station#Replicates TARO(ng gÀ1)TOC(%)Abundance(ind.mÀ2)Biomass(g mÀ2)Number of taxa 1998142199.30.61250 1.0611 1431755.1–2760 3.60171461105.70.691380 3.2321 1999141177.00.70320 1.5014 142390.60.73357 4.7024143392.90.83610 3.78251453123.20.921080 3.4326146192.90.781460 3.9019147124.70.57560 3.0613211111.80.62510 2.1114 2000141167.50.681500.9311 142386.00.74777 2.63311433497.0 2.231023 4.15201453112.70.91553 1.4025146145.20.686808.3021147123.20.74760 4.6219203118.80.6055026.8419204127.30.59340 2.4720211115.50.60710 4.2220212113.50.65450 3.2414 2001141139.30.63690 3.6221 142338.00.66760 3.2731143383.6 1.34590 3.3918145356.60.90710 3.1124146130.60.565307.9716147155.70.8089021.9217203136.90.5812707.3421204147.00.667107.1817211145.50.67970 6.7519212143.20.6010208.4418A.L.Blanchard et al./Marine Pollution Bulletin46(2003)1583–15891585not directly imply a cause and effect relationship,as other unmeasured environmental covariates may be the factors controlling faunal distributions.The observed associations,however,dofit expectations for fauna under the Pearson and Rosenburg model of disturbance (Pearson and Rosenberg,1978).Associations of hydrocarbons and faunal abundance are particularly apparent for six taxa.Three polychae-tes,G.oculata,Melinna cristata,and N.punctata show a lower abundance near the diffuser.G.oculata and M. cristata always occur in low numbers near the diffuser. Numbers of N.punctata were depressed near the diffuser in1999–2000when TARO concentrations were high, and increased substantially with lower TARO concen-trations in2001.G.oculata,is identified as intolerant of petrogenic hydrocarbons(Olsgard and Gray,1995) while another member of the genus Melinna,M.pal-mata,is an indicator species for pollution in European coastal waters(Grehan,1991;Langston et al.,1999). There is no information available for N.punctata al-though some information is published for other members of this family(e.g.,Fauchald and Jumars,1979).The apparent sensitivity of these species to low levels of hy-drocarbons render them particularly useful as indicators of future changes in the spatial distribution of hydro-carbons in Port Valdez.G.oculata(as Myriochele ocu-lata)also shows lower abundance at two stations within the mixing zone,as compared to nearby referenceTable2Abundance values(ind.mÀ2)of numerically dominant taxa in1998–2001Taxon Station14114214319992000200119981999200020011998199920002001 Adontorhina cyclia010503032310609320750 Axinopsida serricata3002040153143479208333027 Capitellidae3002020367105203137 Cirratulidae900300132310720573020 Exogone sp.00003201030330 Galathowenia oculata0201300710270700 Lumbrineris sp.010200102017101037 Melinna cristata1030010713301007 Nephtys punctata30208050405311710507133 Polydora socialis00200350223290170153177 Prionospio steenstrupi1003007871330003 1451461471999200020011998199920002001199920002001 Adontorhina cyclia1039033100802030011010 Axinopsida serricata3834013480310904028019080 Capitellidae67107502020002070 Cirratulidae15733307016030201040150 Exogone sp.33302310130001000 Galathowenia oculata70710107040201030 Lumbrineris sp.137105020101010100 Melinna cristata030000010100 Nephtys punctata573787605080210100100280 Polydora socialis4013322770600100060 Prionospio steenstrupi10333175036030200400203204211212200020012000200119992000200120002001 Adontorhina cyclia2060006030805060Axinopsida serricata20020030120140601605080Capitellidae1001020001000Cirratulidae101002020100180030Exogone sp.10010030030500Galathowenia oculata10250108030804030100Lumbrineris sp.20203020010201030Melinna cristata305020404040801020Nephtys punctata902006010010014013060220Polydora socialis070090010200110Prionospio steenstrupi2050001030700201586 A.L.Blanchard et al./Marine Pollution Bulletin46(2003)1583–1589stations (Blanchard et al.,2002).The thyasirid bivalves Adontorhina cyclia and Axinopsida serricata and the polychaete Polydora socialis (a family and genera known as opportunistic;e.g.,Pearson and Rosenberg,1978)increase in numbers near the diffuser,possibly enhanced by bacteria and particulate organic carbon,as foodinTable 3Correlation values of biological measures and taxon abundance values to total aromatic (TARO)concentrations Variable199920002001r P -value Effect size r P -value Effect size r a P -value Effect size Abundance 0.500.082Medium 0.560.024Medium )0.240.374Small Biomass 0.480.096Medium )0.390.131Medium )0.240.368Small #Taxa)0.120.728Negligible )0.650.007Large )0.640.007Large Adontorhina cyclia 0.490.091Medium 0.84<0.001Large )0.120.667Negligible Axinopsida serricata 0.420.150Small 0.690.003Large )0.270.307Small Capitellidae 0.420.151Small )0.260.925Small 0.050.851Negligible Cirratulidae 0.390.193Small 0.060.838Negligible 0.170.522Negligible Exogone spp.0.170.576Negligible )0.060.820Negligible )0.130.644Negligible Galathowenia oculata )0.840.000Large )0.450.077Medium )0.590.017Medium Lumbrineris sp.)0.210.503Small )0.620.010Medium )0.440.091Medium Melinna cristata )0.780.002Large )0.510.045Medium )0.100.708Negligible Nephtys punctata )0.720.005Large )0.680.004Large )0.260.334Small Polydora socialis0.460.117Medium 0.670.005Large 0.200.464Small Prionospio steenstrupi0.340.261Small)0.150.580Small)0.380.147SmallaRank correlations.A.L.Blanchard et al./Marine Pollution Bulletin 46(2003)1583–15891587diffuser effluent(Blanchard et al.,2002).Beyond basic biological descriptions(e.g.,Scott,1986;Slack-Smith, 1994),little is known about these thyasirid bivalves but Blanchard et al.(2002)suggest that A.serricata (as Axinopsida spp.)may be functioning as an op-portunistic species in Port Valdez(see also Rygg, 1985).Some members of the family Thyasiridae are known to be hosts for chemosymbiotic bacteria that degrade sediment sulphides(Dando and Spiro,1993). Slack-Smith(1994),however,indicates that A.serricata is not a host for these bacteria and Burd(2002)found A. serricata in significantly lower densities in sulphide-rich sediments.The conclusions of our study agree with other re-search projects from Port Valdez.Intertidal studies have rarely identified variations of fauna attributable to ma-rine terminal activities(Feder and Bryson-Schwafel, 1988;Blanchard and Feder,1997,2000a,b).An ex-ception is a small decrease in barnacle abundance fol-lowing a small oil spill in the terminal area in1980 (Rucker,1983).Shaw(1988)discusses accumulations of hydrocarbons in bivalves and sediments in Port Valdez and concludes that decreasing concentrations over time are likely due to better treatment methods of oily ballast water and declining volumes of oil shipments.Recently, Payne et al.(2001)concluded that although a hydro-carbon signature of Alaska North Slope crude oil was found in mussel tissues from within and remote from the marine oil terminal,intertidal and subtidal biota likely experience low stress as a result of treated ballast-water disposal in Port Valdez,as supported by mussel and limpet studies by Blanchard and Feder(1997,2000a,b). Blanchard et al.(2002)concluded that there was a small effect on subtidal infauna due to a short-term and lo-calized increase in sediment hydrocarbons.The use of fixed rather than randomly selected sampling locations in most of the above studies may bias their conclusions. 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