Latitudinal and temporal variability in the community structure and ...

Progress in Oceanography 110 (2013) 80–92Contents lists available at SciVerse ScienceDirectProgress in Oceanographyjournal homepage: www.elsevier.com/locate/poceanLatitudinal and temporal variability in the community structure and fatty acidcomposition of deep-sea nematodes in the Southern OceanKatja Guilini a,⇑ , Gritta Veit-Köhler b , Marleen De Troch a , Dirk Van Gansbeke a , Ann Vanreusel aa Biology Department, Marine Biology Section, Ghent University, Krijgslaan 281/Sterre S8, 9000 Gent, Belgiumb Senckenberg am Meer, DZMB – German Centre for Marine Biodiversity Research, Südstrand 44, 26382 Wilhelmshaven, GermanyarticleinfoabstractArticle history:Available online 11 January 2013This study describes and combines structural and functional aspects of deep-sea nematode assemblagesfrom the Atlantic sector of the Southern Ocean. Samples were collected at six stations along the PrimeMeridian (49–70°S), including a repeated sampling after one and a half months interval at the Polar Front(52°S), where meanwhile a seasonal phytoplankton bloom had settled. The aim was to gain insight in thelatitudinal and temporal variability in nematode community structure and diet based on the genericcomposition and bulk fatty acid composition of the community, respectively. The results show that nematodeassemblages along the transect differed relatively little and that they were all highly comparable toslope and abyssal communities elsewhere in the world in terms of nematode standing stock, diversityand composition. Nematode community composition was only weakly correlated with the communityfatty acid composition, indicating that simply the occurrence of distinct genera or the proportion of nematodefeeding types based on mouth morphology, cannot explain the variance in FA compositions of thecommunities. Moreover, the generally low FA content of nematodes suggests that they do not accumulatelipids for energy storage and that they may feed throughout the year on constantly available food sources.A year-round foraging activity could also explain the recorded lack of food uptake as a short-termresponse to the recently settled phytodetritus at the revisited Polar Front station. Nevertheless, the higherrelative abundance of nematodes in the top centimeter layer of the sediment and the occurrence of thegenus Leptolaimus only after phytodetritus had settled at the seafloor, suggests the recording of an earlystage in a delayed response to the seasonal event.Ó 2013 Elsevier Ltd. All rights reserved.1. IntroductionSimilar to other ocean basins, the benthos in the SouthernOcean (SO) deep sea (i.e. >1000 m of water depth) is poorly knownin comparison with the continental shelf (Clarke and Johnston,2003; Clarke, 2008). Moreover, although metazoan meiofauna representan ubiquitous group of organisms, numerically dominantcompared to other metazoans at all water depths (Rex et al.,2006; Wei et al., 2010), diversity and ecosystem roles played bymega- and macrofauna are far better documented. Ecological studieson SO metazoan meiofauna so far have shown that the communitiesfollow a general pattern of decrease in abundance withincreasing water depth and generally decreasing food availabilityalong the continental shelf and slope (Herman and Dahms, 1992;Vanhove et al., 1995; Gutzmann et al., 2004). This corresponds toa pattern found for metazoan meiobenthos in the deep sea worldwide(Mokievskii et al., 2007). As documented by a large number ofstudies (reviewed by Heip et al. (1985) and Giere (2009)), sedimentproperties and food availability were both of prime importance in⇑ Corresponding author. Tel.: +32 9 264 85 31; fax: +32 9 264 85 98.E-mail address: Katja.Guilini@UGent.be (K. Guilini).explaining the composition of the Antarctic deep-sea meiofauna,particularly nematode communities (Herman and Dahms, 1992;Vanhove et al., 1995, 2004). Apart from water depth, other multiple,interdependent factors such as hydrography, topography, icecoverage, light, temperature, nutrient availability and the structureof the pelagic food web influence the food supply that reaches theseafloor (Grebmeier and Barry, 1991; Bathmann et al., 1997; Clarkeand Arntz, 2006; Arrigo et al., 2008). Because of the occurrence ofthe Polar Front, seamounts, and a seasonally retreating ice zone,the SO is characterized by latitudinal and seasonal variations in organiccarbon fluxes reaching the seafloor (Sachs et al., 2009), whichmay result in spatial and temporal variability in benthic standingstocks.Mounting evidence on the presence of seasonal detritus depositionsin the deep sea came along with contrasting findings on benthicresponses to the deposition of phytodetritus (e.g. Billett et al.,1983; Graf, 1992; Gooday et al., 1996; Soetaert et al., 1996; Drazenet al., 1998). Although deep-sea meiofaunal standing stock is generallyproportional to food availability (i.e. sediment organic carboncontent and chloroplastic pigment equivalents (CPE); e.g.Vanreusel et al., 1995; Soetaert et al., 2009), the response in termsof food uptake or community shifts of nematodes to both natural0079-6611/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.pocean.2013.01.002

K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92 81and experimentally simulated depositions of phytodetritus is onlyminimal or absent compared to bacteria, foraminiferans and severalmacrofaunal taxa (e.g. Gooday, 1988; Graf, 1992; Pfannkuche,1993; Soltwedel, 1997; Galéron et al., 2001; Guilini et al., 2010 andreferences therein). The only rapid responses found to an episodicfood supply in the deep sea were an increase in mean nematodesize at the German BIOTRANS site (April–July; Soltwedel et al.,1996) and nematode migration towards the sediment surface inthe Polar Front (December–January; Veit-Köhler et al., 2011). Doubledmeiofaunal abundance (mainly nematodes), from summer toautumn in sediments from the bathyal Mediterranean (de Bovéeet al., 1990) and the Northeast Atlantic along the Hebridean margin(Mitchell et al., 1997) indicate, however, a response on a longertime scale. Therefore, it is speculated that deep-sea nematodesare feeding additionally or alternatively on rather unlimited, otherfood sources than phytodetritus (e.g. bacteria, ciliates, flagellates,foraminiferans, fungi, DOC) and that they may be characterizedby generally slower rates of colonization, respiration and somaticgrowth (Guilini et al., 2010, 2011). Rigid evidence that any of thesefood sources are of substantial importance to maintain the metabolicdemands of nematodes, or respiration measurements underin situ conditions are, however, lacking.This study describes and combines both structural and functionalaspects of deep-sea nematode assemblages along a latitudinaltransect following the Prime Meridian across the SO (49–70°S).Besides a spatial scale, a temporal scale was considered with regardsto the short-term response of nematode assemblages to aseasonal deposition of particulate organic matter (POM). Therefore,a station located in the Polar Front (52°2 0 S, 0°1 0 W), where a phytoplanktonbloom had settled during the course of the expedition,was revisited after 52 days to perform repeated measurements.Overall, structural aspects comprise standing stocks and communitycomposition, while functional aspects refer to feeding ecology,which is investigated by means of fatty acid (FA) compositions.Nematode FA compositions are determined to provide a time-integratedview on the organisms’ diets at the community level. The FAmarker concept relies on the fact that certain FA are incorporatedinto consumers in a conservative manner (e.g. Dalsgaard et al.,2003; Lee et al., 2006). By comparing nematode FA with what isknown from literature on surface water POM, other benthic organisms,bulk sediment and bottom-water POM properties, we aim toprovide insights as to the resources used by deep-sea nematodecommunities across the Southern Ocean. Although this techniqueis widely spread in marine ecological studies (see review by Kellyand Scheibling (2012)), it was only applied three times on marinefree-living nematodes (Leduc, 2009; Leduc and Probert, 2009; VanGaever et al., 2009).The following hypotheses were tested:(1) Structural and functional characteristics of deep-sea nematodeassemblages do not differ along a latitudinal gradientacross the SO.(2) Deep-sea nematodes at the Polar Front do not respond to aseasonal pulse of organic matter to the seafloor.2. Materials and methods2.1. Study site and sampling procedureSamples were collected during the ANDEEP-SYSTCO expeditionon board of the RV Polarstern (ANT XXIV/2, 28.11.2007–04.02.2008). Sediment samples were taken at depths from1935 to 5323 m, at six sites along a north–south gradient, inclose proximity of the Prime Meridian between 49°S and 70°S;across the Polar Front, the Weddell Sea and the Lazarev Sea(Fig. 1, Table 1). The stations are further indicated with theirabbreviations (PF: Polar Front, sPF: south Polar Front, cWS: centralWeddell Sea, MR: Maud Rise, LS: Lazarev Sea). All stationsoccur in different water masses and environments with differenttopographical, sedimentary and productivity conditions. The PF,sPF and cWS station are situated on the abyssal sea floor, MRis a seamount and LS is located at the continental slope. The stationlocated at a southern position in the Polar Front (sPF, at52°S) was visited twice; once when a phytoplankton bloomwas detected in the euphotic water layer based on increasedfluorescence levels (06.12.2007; Herrmann and Bathmann,2010) and 52 days later when the remains of the bloom had settledto the sea floor (26–27.01.2008). These remains were visibleas a greenish fluff layer on the sediment surface (Veit-Köhleret al., 2011). Sachs et al. (2009) calculated the labile portion ofthe organic carbon flux (LC org ) based on in situ and ex situ measurementsof O 2 profiles in surface sediments (Table 1).All meiobenthic samples were taken with a multiple corer(MUC) sampling device equipped with 12 plexiglass cores (innerdiameter: 9.4 cm, equivalent to 69.4 cm 2 ). The MUC was deployedone to three times per station, depending on ship time availabilityand sea state. The processed samples were thus a combination oftrue replicates and pseudo-replicates, since different cores fromthe same MUC deployment do not meet the criteria of randomsampling (Hurlbert, 1984). An overview of the processed samplesis given in Table 1. The single MUC deployment at the Polar Frontstation was only partially successful. It was visually determinedthat some cores were disturbed. The most undisturbed cores werereserved for FA analysis, in order to ensure enough organismscould be collected. From all stations, the sediment cores destinedfor meiofauna community analysis were sliced into 1-cm fractionsdown to 5 cm and together with the supernatant water preservedin a borax-buffered 4% formaldehyde-seawater solution. Furthermore,a minimum of four cores per deployment were used to scoopoff the upper 5 cm of sediment. This material was immediatelysieved in the lab with filtered seawater (32 lm mesh) over stackedsieves (1 mm, 500 lm, 100 lm and 32 lm) to prevent clogging.The retained 500 lm, 100 lm and 32 lm fractions were pooledand stored at 80 °C. Back at the laboratory, the nematodes wereextracted for fatty acid analyses.2.2. Nematode parametersSediment samples destined for identifying the nematode communitywere rinsed with tap water over a 32 lm mesh sieve (noupper sieve size used). The fraction retained on the 32 lm sievewas three times centrifugated with the colloidal silica polymerLevasil Ò (H.C. Stark, 200/40%, q = 1.17, for 6 min at 4000 rpm)and kaolin (McIntyre and Warwick, 1984) to extract all organisms.After staining with Rose Bengal, all metazoan organisms weremanually sorted to higher taxon level (following Higgins and Thiel,1988) and counted under a Leica MZ 12.5 stereomicroscope (8–100 magnification). Where possible, about 50–100 nematodeswere picked out randomly with a fine needle from each centimetersediment layer. They were gradually transferred to glycerine (Seinhorst,1959) before being mounted on glass slides. Nematodeswere identified to genus level under a compound microscope(1000 magnification). Adults were distinguished from juvenilesbased on the development of a vulva and uterus in females and agonad and spicules in males. Based on mouth morphology, all identifiedindividuals were classified into four feeding type groupsaccording to Wieser (1953): selective deposit feeders (1A), nonselectivedeposit feeders (1B), epistratum feeders (2A), and predators/scavengers(2B). By using a Leica DMR compound microscopeand Leica LAS 3.3 imaging software, nematode length (L, filiformtail excluded) and maximal width (W) were measured. Nematode

82 K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92Fig. 1. Location of the ANDEEP-SYSTCO stations. (A) Bathymetric map situating the stations across the Southern Ocean, along the Prime Meridian. Exact coordinates are givenin Table 1. The map shows following features of the Antarctic Circumpolar Current: Subtropical Front (STF), Subantarctic Front (SAF), Southern Antarctic Circumpolar CurrentFront (sACCf), Polar Front (PF), Southern Boundary of the Antarctic Circumpolar Current (sbACC) (Orsi et al., 1995). (B) Cross-section of the bathymetry along the transect withindication of the stations. Bathymetry data provided by ETOPO1 (Amante and Eakins, 2009).Table 1Overview of the ANDEEP-SYSTCO stations, deployments per station and core codes of the samples that were processed for meiofaunal densities and additionally for nematodecommunity composition, diversity and biomass (in bold). Date, depth, longitude and latitude are listed. Per station, the labile portion of the organic carbon flux (LC org ), ascalculated by Sachs et al. (2009) based on in situ and ex situ measurements of O 2 profiles in surface sediments, is shown.Location Station-deployment (core code) Date Depth (m) Latitude Longitude LC org flux (mg C m 2 d 1 )PF 090-2 (2–8) 29.01.2008 3980 49°0.95 0 S 0°0.03 0 E 2.4sPF 013-12 (2–6–12) 06.12.2007 2963 52°2.22 0 S 0°1.04 0 W 3.3sPF 013-14 (1–4–9) 06.12.2007 2970 52°2.25 0 S 0°1.11 0 WsPF (2nd visit) 085-5 (2–3–11) 26.01.2008 2965 52°1.20 0 S 0°0.20 0 E 8.4 ± 1.0sPF (2nd visit) 085-7 (1–4–8) 27.01.2008 2964 52°1.53 0 S 0°0.16 0 EcWS 033-10 (3–4) 30.12.2007 5323 62°0.80 0 S 2°59.05 0 W 3.0MR 039-10 (5) 03.01.2008 2116 64°28.83 0 S 2°52.48 0 E 2.1 ± 0.4MR 039-12 (8) 03.01.2008 2123 64°28.83 0 S 2°52.53 0 EMR 039-14 (11) 03.01.2008 2119 64°28.84 0 S 2°52.49 0 ELS 017-12 (6–8–11) 22.12.2007 1935 70°4.86 0 S 3°22.59 0 W 2.0LS 017-14 (1–11–12) 22.12.2007 1951 70°4.80 0 S 3°22.71 0 Wbiomass was then calculated with Andrassy’s formula (Andrassy,1956): wet weight (lg) = L (lm) W 2 (lm)/1.6 10 6 , and a dryto-wet-weightratio of 0.25 was assumed (Heip et al., 1985). To calculatetotal biomass of each sediment layer and sampling station,total nematode densities were taken into account.Samples that were stored frozen for fatty acid analyses werethawed and triple centrifugated with Levasil Ò and kaolin (6 minat 4000 rpm) to extract the meiofauna. The extracted meiofauna(size range: 1 mm to 32 lm) was rinsed with MilliQ water and processedimmediately. Two to three times 300–550 bulk nematodeindividuals per station (equaling minimum 33.1 lg to maximum193.3 lg dry weight) were handpicked with a fine sterile needle.After rinsing in MilliQ water to remove adhering particles theywere transferred in MilliQ water into 4.0 ml GC vials with a

K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92 83minimum of MilliQ water and frozen again at 80 °C before freezedrying.Hydrolysis of total lipids and methylation to fatty acidmethyl esters (FAME) for FA analysis was achieved by a modifiedone-step derivatisation method after Abdulkadir and Tsuchiya(2008). The boron trifluoride-methanol reagent was replaced by a2.5% H 2 SO 4 -methanol solution since BF 3 -methanol can cause artefactsor loss of polyunsaturated FA (PUFA; Eder, 1995). The fattyacid methylnonadecanoate C19:0 (Fluka 74208) was added as aninternal standard for the quantification. Samples were centrifuged(Eppendorf centrifuge 5810R) and vacuum dried (Rapid Vap LAB-CONCO). The FAME obtained from the replicate extracts of thenematodes in each of the five locations were analyzed using agas chromatograph (Hewlett Packard 6890N) coupled to a massspectrometer (HP 5973). All samples were run in splitless mode,with a 5 lL injection per run, at an injector temperature of250 °C, using a HP88 column (60 m 25 mm internal diameter,Df = 0.20; Agilent J&W; Agilent Co., USA) with He flow rate of1.3 ml min 1 . The oven temperature was programmed at 50 °Cfor 2 min, followed by a ramp at 25 °C min 1 to 75 °C, then a secondramp at 2 °C min 1 to 230 °C with a final 4 min hold. FAMEwere identified by comparison with the retention times and massspectra of authentic standards and available ion spectra in WILEYmass spectral libraries, and analyzed with the software MSDChemStation (Agilent Technologies). Quantification of individualFAME was accomplished by the use of external standards (SupelcoTM37 Component FAME Mix, Supelco # 47885, Sigma–AldrichInc., USA). The quantification function of each individual FAMEwas obtained by linear regression applied to the chromatographicpeak areas and corresponding known concentrations of the standards(ranging from 5 to 150 lgmL 1 ). Shorthand FA notationsof the form A:BxX were used, where A represents the number ofcarbon atoms, B gives the number of double bonds and X is the positionof the double bond closest to the terminal methyl group(Guckert et al., 1985). Some FA, used as biomarkers for the typeof ingested food, are of special interest and widely used for theinterpretation of an organism’s FA composition. Therefore wegrouped the planktonic markers 16:1x7, 18:1x9, 18:2x6,20:PUFA, 22:PUFA; and the bacterial markers 15:0, 17:0, 15:1,17:1, iso and anteiso-branched SFA and MUFA, 10-methylpalmiticacid, 16:1x7t, 18:1x7c, cy17:0 and cy19:0 (e.g. Dalsgaard et al.,2003 and references therein; Camacho-Ibar et al., 2003 and referencestherein; Desvilettes et al., 1997; Gurr and Harwood, 1991).2.3. Statistical analysisStatistical analyses were conducted using PRIMER version 6with PERMANOVA+ add-on software (Clarke and Gorley, 2006;Anderson et al., 2008). Prior to the analyses, nematode densityand biomass data of the upper 5 cm layers were summed takinginto account the individual counts per depth layer. Structuraldiversity was assessed with Hill’s indices that are variably dependenton relative genera abundances and thus cover both genusrichness and evenness (H 0 = number of genera, H 1 , H 2 , H inf ; Hill,1973; Heip et al., 1998). Additionlly, a rarefaction index, i.e. the expectednumber of genera present in a population of 100 individuals(EG(100); Hurlbert, 1971), was generated. To assess functionaldiversity, the trophic diversity index H 1 was calculated (Heipet al., 1988). Along the transect both univariate and multivariatenon-parametric permutational ANOVAs (PERMANOVA) were performedto test for differences in nematode density, biomass, diversity,FA content and nematode genus and FA composition,respectively. One replicate fatty acid sample (cWS) was omittedfrom the dataset due to exorbitant high measured concentrationscompared to the other samples. Euclidean distance similarity wasused as resemblance measure on untransformed univariate data,while Bray–Curtis similarity was used as resemblance measureon standardized and square root or log(x + 1) transformed genusabundances and FA relative percentages, respectively. Both modelshad an unbalanced one factor design including the fixed categoricalfactor ‘location’. Calculation of the Pseudo-F ratio and p value requiredunrestricted permutation of raw data (univariate) or 9999permutations of the residuals under a reduced model (multivariate).Post-hoc pairwise tests were only performed after PERMDISPconfirmation of homogeneity of multivariate sample dispersionand clarified between which locations or sediment depth layersthat the significant differences identified by the main tests werefound. Because of the restricted number of unique permutationsin the pairwise tests, p values were obtained from Monte Carlosamplings (Anderson and Robinson, 2003). A non-metric multidimensionalscaling (MDS) plot was constructed to visualize thenematode community composition among all stations. To visualizethe differences in nematode FA compositions among the stations aPrincipal Coordinates analysis (PCO) was used. PCO is comparableto MDS in that it is very flexible – it can be based on any (symmetric)resemblance matrix. However, it is also like a PCA, in that it is aprojection of the points onto axes that minimize residual variationin the space of the resemblance measure chosen. Due to the limitedsample-to-variable ratio, variables represented by less than fivesamples were deleted to improve the reliability and reproducibilityof the analysis as proposed by Tabachnick and Fidell (1989) for PCAanalyses (Budge et al., 2006). In addition, a new feature provided aspart of the PERMANOVA+ add-on is the ability to superimposevectors onto the plot that correspond to the raw correlations ofindividual variables with the ordination axes. We chose the Spearmanrank correlation that shows monotonic increasing or decreasingrelationships with axes. The vector overlay includes only thoseFA that correlated with more than 60% with one of the first twoPCO-axes. Additionally a RELATE analysis on replicate samples,based on the Spearman rank method, was used to test for a correlationbetween the nematode community composition (genericand trophic) and fatty acid composition at all stations.To test the effect of a settled phytoplankton bloom on differentnematode parameters (community composition, total and meanindividual biomass, juvenile versus adult ratio) over 5 cm depthat the sPF station, multivariate and univariate PERMANOVA analyseswith a balanced fully crossed three factor design were used.The model included the fixed categorical factors ‘time’ and ‘sedimentdepth’ with the random ‘replicate’ factor nested in ‘time’(since data from different depth layers from a single replicate coreare not fully independent), and all interaction terms. Both multivariateand univariate analysis were run as described above.3. Results3.1. Latitudinal variability across the Southern Ocean3.1.1. Nematode community structureNematodes dominated the metazoan meiofauna at all locations,with a dominance ranging from 80.5 ± 3.3% to 92.6 ± 0.3% (Table 2).Nematode densities ranged from 69 ± 5 ind. 10 cm 2 to1102 ± 233 ind. 10 cm 2 , with lowest densities found at the PF stationand highest at the MR station. Nematode biomass ranged from11.3 ± 2.6 lg dwt 10 cm 2 at the PF station to 324.1 ± 175.5 lg dwt10 cm 2 at the MR station. The curiously low mean density andbiomass at the Polar Front station confirm what was visually determinedon board, i.e. that the samples were disturbed in the courseof the sampling process. Therefore, nematode standing stocks ofthe PF station were not included in the analyses. PERMANOVAfound significantly lower nematode densities at the sPF stationcompared to the MR station and at the sPF revisited station comparedto the stations cWS, MR and LS (Table 3). Significant

84 K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92Table 2Nematode relative abundance, density, biomass, diversity (H 0 , H 1 , H 2 , H inf , EG(100)) and relative abundance of the nematode feeding types and trophic diversity (H 1 ) for the top5 cm of the sediment, averaged per location (± standard deviation).LocationNematode relativeabundance (%)Nematode density(ind. 10 cm 2 )Nematode biomass(lg dwt 10 cm 2 )H 0 H 1 H 2 H inf EG(100) Feeding types H 11A 1B 2A 2BPF 90.9 ± 0.1 69 ± 5 11.3 ± 2.6 49.5 ± 4.9 24.7 ± 2.5 14.2 ± 0.4 5.7 ± 0.0 35.8 ± 2.5 53 ± 2 16 ± 1 24 ± 4 8 ± 1 2.7 ± 0.1sPF 85.5 ± 2.6 693 ± 258 105.7 ± 11.5 55.3 ± 2.9 26.5 ± 1.0 17.5 ± 2.0 7.8 ± 1.4 34.6 ± 1.0 30 ± 5 22 ± 1 42 ± 4 6 ± 2 3.1 ± 0.1sPF (2nd visit) 80.5 ± 3.3 480 ± 48 62.5 ± 21 54.3 ± 3.1 26.5 ± 1.4 17.3 ± 0.9 7.4 ± 0.8 33.5 ± 2.5 30 ± 7 15 ± 1 51 ± 6 4 ± 1 2.6 ± 0.1cWS 92.3 ± 2.8 648 ± 145 159.0 ± 58.3 47.5 ± 0.7 18.8 ± 1.1 10.4 ± 0.2 4.2 ± 0.1 28.8 ± 0.6 28 ± 2 43 ± 4 26 ± 0 3 ± 2 3.0 ± 0.2MR 92.6 ± 0.3 1102 ± 233 324.1 ± 175.5 45.3 ± 3.2 24.2 ± 3.7 17.2 ± 3.3 7.2 ± 0.9 33.7 ± 2.4 24 ± 2 17 ± 1 51 ± 4 9 ± 3 2.9 ± 0.2LS 86.4 ± 2.5 833 ± 132 294.5 ± 145.7 57.0 ± 1.0 30.8 ± 3.0 21.7 ± 3.8 9.5 ± 2.7 39.0 ± 1.0 29 ± 6 28 ± 6 33 ± 4 11 ± 2 3.5 ± 0.1differences in biomass were only detected between both samplingtimes at the sPF station (Table 3).A total of 137 genera belonging to 36 families were identified.An overview of the dominant genera per station, with a relativeabundance higher than 2%, is given in Table 4. The four genera thatdominate at all stations, though with varying abundances, are Desmoscolex(16.8–3.3%), Acantholaimus (13.5–6.2%), Tricoma (6.8–2.3%) and Halalaimus (7.9–2.8%). Only between 6.0% and 16.6% ofthe genera were present with abundances lower than 1%. The percentageof genera that occurred exclusively at one station rangedfrom 2.1% at the MR station to 9.0% at the LS station. These exclusivegenera only accounted for 0.4–2.7% of the total abundances.PERMANOVA results showed that the nematode assemblages differedamong the stations (Table 3). Pairwise comparisons revealedthat significant differences were only found between the stationMR and all other stations, except for the sPF station; and betweenthe stations sPF (2nd visit) and cWS and LS (Table 3). These resultswere visualized in an MDS plot (Fig. 2).Diversity indices differed significantly among the stations (Table3). Since no consistent pattern among the stations occurred,due to varying relative abundances of rare genera, the averagediversity measures are interpreted. Average structural diversityindices were all highest for the LS station (Table 2), regardless ofthe emphasis given to relatively more or less abundant genera. Besidesthe highest average number of genera (H 0 = 57 ± 1) andexpected number of genera on 100 individuals (EG(100) = 39 ± 1),genera also occurred most evenly (H inf = 9.5 ± 2.7), withAcantholaimus being the most dominant genus (9.2%). While thelowest number of genera was found at the MR station(45.3 ± 3.2), Hill’s diversity indices indicated lowest evenness dueto highest dominance of one genus (Theristus: 23.9%) at the deepeststation, cWS. In terms of evenness, diversity more or less decreasedwith water depth.Based on mouth morphology, nematode assemblages weredominated by epistratum feeders at most stations (sPF: 42 ± 4%,sPF (2nd visit): 51 ± 6%, MR: 51 ± 4% and LS: 33 ± 4%), followedby selective deposit (24 ± 2% to 30 ± 5%) and non-selective depositfeeders (15 ± 1% to 28 ± 6%). At the PF station the proportion of epistratum(24 ± 4%) and selective deposit feeders (53 ± 2%) was reversed,while at the cWS station non-selective deposit feedersdominated (43 ± 4%), followed by epistratum (28 ± 2%) and selectivedeposit feeders (26%) (Table 2). Predators and scavengershad the lowest abundances at all stations (3 ± 2% to 11 ± 2%). Trophicdiversity ranged from 2.6 ± 0.1 at the sPF (2nd visit) station to3.5 ± 0.1 at the LS station (Table 2), with a significantly higher trophicdiversity at the LS station compared to all other stations(Table 3).3.1.2. Nematodes fatty acid compositionsAt all stations, PUFA dominated in nematodes (34.2% to45.3 ± 9.5%; Table 5). When FA markers were allocated to the potentialfood source, planktonic FA (R 16:1x7c, 18:1x9, 18:2x6,Table 3Results from main and pairwise one-factor multivariate and univariate PERMANOVA analyses testing for differences in nematode community composition, nematode fatty acidcomposition and nematode density, biomass, structural diversity and functional diversity, and nematode d 13 C and d 15 N values, respectively, in the top 5 cm of the sedimentamong all locations. Significant differences are indicated in bold.FactorNematodedensityNematodebiomassNematodecommunityNematode diversityH 0 H 1 H 2 H inf EG(100) H 1Location df 4 4 5 5 5 5 5 5 5 5MS 1.0 10 7 39667 1758 62.2 37.4 34.2 7.8 26.7 0.3 253.1Pseudo-F 6,6857 a 3.29 3.33 b 7.49 a 6.41 a 5.67 a 3.71 a 7.75 a 12.67 a 4.31 bResiduals df 18 9 10 10 10 10 10 10 10 13MS 1.5 10 6 12072 528.6 8.3 5.8 6.0 2.1 3.4 0.02 58.7Total df 22 13 15 15 15 15 15 15 15 18PF, sPF t – – 1.86 1.73 1.20 2.22 2.07 0.78 4.04 b 1.75PF, sPF (2nd visit) t – – 1.85 1.40 1.04 4.45 a 2.98 1.00 0.57 2.15PF, cWS t – – 1.85 0.57 3.06 12.56 a 20.4 a 3.86 2.37 1.19PF, MR t – – 2.19 a 1.18 0.17 1.25 2.21 0.95 1.16 2.34 aPF, LS t – – 1.81 2.76 2.35 2.65 1.85 2.15 10.33 a 3.71 asPF, sPF (2nd visit) t 1.67 3.06 a 1.03 0.41 0.03 0.14 0.48 0.72 4.54 b 1.67sPF, cWS t 0.08 1.67 1.66 3.59 a 8.42 a 4.75 a 3.56 a 7.14 a 0.93 1.20sPF, MR t 2.72 a 2.15 1.78 4.01 a 1.06 0.12 0.73 0.63 1.49 1.57sPF, LS t 1.57 2.24 1.53 0.94 2.38 1.71 0.92 5.40 a 4.04 b 2.60 asPF (2nd visit), cWS t 2.59 a 2.78 2.02 a 2.96 6.34 a 9.97 a 5.67 a 2.46 2.77 1.56sPF (2nd visit), MR t 6.10 b 2.56 1.91 a 3.52 a 1.01 0.05 0.37 0.09 1.72 1.88 asPF (2nd visit), LS t 5.52 b 2.73 1.80 a 1.44 2.27 1.95 1.26 3.56 a 9.42 a 3.36 acWS, MR t 2.40 1.23 2.33 a 0.89 1.93 2.79 4.55 a 2.66 0.54 1.13cWS, LS t 1.66 1.20 1.75 11.4 a 5.22 a 3.96 a 2.61 12.61 a 4.49 b 2.75 aMR, LS t 2.26 0.58 2.13 a 6.00 a 2.43 1.56 1.40 3.55 a 4.26 b 2.48 aa 0.001 < p 6 0.05.b p 6 0.001Nematodefatty acids

K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92 85Table 4Mean relative abundance of dominant genera (>2%) per station, over 5 cm sediment depth.PF % sPF % sPF (2nd visit) % cWS % MR % LS %Desmoscolex 16.8 Acantholaimus 13.0 Acantholaimus 12.4 Theristus 23.9 Actinonema 11.7 Acantholaimus 9.2Acantholaimus 13.5 Daptonema 8.1 Microlaimus 10.6 Acantholaimus 11.5 Desmodora 11.4 Sabatieria 8.8Tricoma 6.8 Halalaimus 7.9 Chromadorina 8.0 Desmoscolex 7.8 Microlaimus 6.6 Desmoscolex 6.9Monhystrella 6.1 Actinonema 6.3 Halalaimus 6.0 Daptonema 7.8 Acantholaimus 6.2 Dichromadora 5.1Halalaimus 4.0 Desmoscolex 5.6 Actinonema 4.6 Halalaimus 4.5 Chromadorina 5.9 Cervonema 4.7Gammanema 3.5 Desmodorella 4.4 Tricoma 4.6 Dichromadora 4.2 Paramesacanthion 5.4 Daptonema 4.7Leptolaimus 3.5 Monhystrella 4.3 Monhystrella 4.5 Tricoma 4.1 Enchonema 3.8 Chromadorina 3.5Prototricoma 3.3 Chromadorina 4.0 Desmoscolex 4.1 Monhystrella 3.3 Dichromadora 3.5 Halalaimus 3.3Diplopeltoides 2.9 Tricoma 3.5 Daptonema 3.7 Intasia 3.0 Leptolaimus 3.5 Microlaimus 3.3Procamacolaimus 2.2 Pselionema 2.9 Desmodora 3.3 Microlaimus 2.7 Thalassomonhystera 3.4 Intasia 2.9Microlaimus 2.9 Leptolaimus 3.0 Enchonema 2.2 Desmoscolex 3.3 Bolbolaimus 2.8Intasia 2.5 Intasia 3.0 Prototricoma 2.2 Halalaimus 2.8 Desmodorella 2.6Paracantonchus 2.5 Paracantonchus 2.9 Leptolaimus 2.1 Tricoma 2.5 Tricoma 2.3Desmodora 2.2 Pselionema 2.7 Pselionema 2.1 Actinonema 2.1Desmodorella 2.4 Theristus 2.0Rest 37.5 Rest 29.8 Rest 24.2 Rest 20.5 Rest 27.9 Rest 35.73.2. Temporal variability at the south Polar FrontFig. 2. Non-parametric multi-dimensional scaling (MDS) plot of the nematodecommunities in the top 5 cm of the sediment along the ANDEEP-SYSTCO transect.20:PUFA, 22:PUFA) were dominant in nematodes at all stations,with values varying from 59.4 ± 3.0% at the sPF station to67.6 ± 3.7% at the PF station. Only a few conventional bacterialFA biomarkers were found in the nematodes (15:0, 17:0,17:1x7c). Together they accounted for a maximum of 5.7 ± 0.9%of the total amount of FA at the PF station. The predominant individualfatty acids that reached more than 10% relative abundanceat one of the stations were 14:0, 16:0, 18:1x9t, 18:1x9c,20:4x6, 20:5x3, and 22:6x3. Total FA content of nematodes, expressedas the percentage of dry weight, varied from 0.29 ± 0.03%at the PF station to 6.21 ± 4.4% at the cWS station (Table 5), withsignificant differences only found between the stations PF andMR (Pairwise test, P(perm) = 0.038) and between LS and MR (Pairwisetest, P(perm) = 0.005). The PERMANOVA analysis also indicateda difference in FA composition between the LS station andall other stations, and between the MR station and the PF andsPF (2nd visit) stations (Table 3). The PCO analysis explained54.5% of total variance in FA compositions of nematodes in the firsttwo axes (29% and 25.5%, respectively) (Fig. 3). The vector overlayindicates FA-specific correlation of more than 60% with one of thefirst two PCO axes, and thus identifies which FA are characteristicfor the observed patterns in the ordination. The most obvious findingis that nematodes from the LS station differed from all otherstations mainly due to increased levels of the FA 16:1x7c, 14:0,20:5x3 and 20:0 (Fig. 3, Table 5). According to the RELATE analysisnematode fatty acid compositions were only poorly correlated tonematode community composition, both on generic (rho = 0.304,p = 0.04) and trophic level (rho = 0.491, p = 0.02).Between pre- and post-settlement of the phytoplankton bloom,the nematode community composition did not change (Table 3).This was also the case when PERMANOVA considered each centimeterseparately (Table 6). At the sPF station Acantholaimus wasthe most dominant genus before (13.0%) as well as after (12.4%)the bloom had settled (Table 4). All other dominant genera that occurredat the pre-bloom situation remained dominant over time,although with small variations in relative abundances. Leptolaimus,however, only appeared after the bloom had settled (3.0%, Table 4).Although total nematode densities per centimeter layer did notchange with time (Table 6), a significantly higher portion of nematodeswas found in the top centimeter after compared to beforethe bloom had settled (44.5 ± 7.5% versus 32.8 ± 10%, respectively;Fig. 4, Table 6). A significant difference in total nematode biomasswas found based on the interaction term ‘Time Sediment depth’(Fig. 4, Table 6). Nevertheless, a PERMDISP analysis revealed thatthis difference was due to a difference in relative data dispersionbetween the two sampling times. Therefore no valid pairwise comparisonbetween the different sediment depth layers of the differentsampling times could be performed. Mean individual biomassof nematodes and the relative proportions of juveniles and adultsdid also not change over time (Table 6).4. Discussion4.1. Latitudinal variability across the Southern Ocean4.1.1. Nematode community structureThe dominance of nematodes in meiofaunal assemblages is inaccordance with other observations in the SO (Herman and Dahms,1992; Vanhove et al., 1995, 2004; Gutzmann et al., 2004), and correspondsto a broad range of deep-sea sediments throughout theworld’s oceans (Mokievskii et al., 2007). Along the latitudinal AN-DEEP-SYSTCO transect, however, nematode relative proportionsamong the meiofauna as well as meiofaunal densities and nematodestanding stock did not consistently decrease with water depthas usually found along continental slopes. We rather suggest that,along the transect, the variable productivity and water depth, areinteracting driving forces that determine nematode standingstocks. Nevertheless, most of the meiofaunal densities are situatedslightly above the World Ocean’s regression line provided in Soltwedel(2000) and Wei et al. (2010). Likewise, nematode biomass isrelatively high compared to areas worldwide at similar depths(Mokievskii et al., 2007).

86 K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92Table 5Relative concentrations of individual FA (% of total FA) in nematodes from all ANDEEP-SYSTCO stations: saturated FA (SFA), monounsaturated FA (MUFA), polyunsaturated FA(PUFA). FA of planktonic and bacterial origin and the ratios of FA 16:1x7/16:0 and 20:5x6/22:6x3 are reported as biomarkers. Total dry weight (lg), FA concentration (lg/350 llextract) and the fraction of total FA versus nematodes dry weight are given for the total number of nematode individuals analyzed per sample. All concentrations and ratios areexpressed as average ± standard deviation of P2 (pseudo-)replicates.PF sPF sPF (2nd visit) cWS MR LSPS 71/90 PS 71/13 PS 71/85 PS 71/33 PS 71/39 PS 71/1712:0 0.7 ± 0.9 0.9 ± 0.2 0.5 ± 0.2 1.7 0.6 ± 0.2 0.4 ± 0.114:0 3.3 ± 0.3 5.7 ± 1.7 4.8 ± 0.9 5.1 4.1 ± 0.8 11.0 ± 2.114:1x5c – – 1.2 ± 1.1 – – –15:0 1.7 ± 0.9 1.4 ± 0.8 1.0 ± 0.5 0.7 1.0 ± 0.1 0.5 ± 0.216:0 7.7 ± 1 11.8 ± 3.9 10.2 ± 3.5 6.3 7.5 ± 3.3 10.6 ± 1.916:1x7c 2.2 ± 0.5 3.5 ± 2.0 4.0 ± 3.4 3.6 3.1 ± 1.3 6.0 ± 0.617:0 2.6 ± 2 4.3 ± 0.1 3.0 ± 0.5 2.1 2.5 ± 0.7 1.4 ± 0.317:1x7c – – 0.4 ± 0.6 – – –18:0 4.9 ± 0.2 7.4 ± 0.8 5.4 ± 0.6 3.9 5.6 ± 0.9 3.4 ± 0.418:1x9t 13.6 ± 4.4 7.2 ± 2.9 7.0 ± 1.2 8.7 7.7 ± 1.4 10.9 ± 0.818:1x9c 8.6 ± 0.01 8.2 ± 1.4 8.8 ± 1.4 10.1 6.6 ± 0.8 10.1 ± 0.518:2x6t 3.7 ± 5.2 – – – 0.9 ± 1.8 –18:2x6c 6.0 ± 1.8 1.0 ± 0.6 1.3 ± 0.4 2.9 1.8 ± 0.2 2.1 ± 0.820:0 – 0.7 ± 1.1 – 1.6 0.6 ± 1.5 2.5 ± 0.220:1x9t 2.8 ± 1.6 1.9 ± 0.6 1.8 ± 0.5 3.0 2.2 ± 1.0 2.5 ± 0.620:1x9c 3.0 ± 0.1 2.4 ± 1.4 3.3 ± 0.9 3.8 2.8 ± 0.5 2.5 ± 0.820:2x6 3.1 ± 1.6 1.4 ± 0.3 1.2 ± 0.7 3.4 3.7 ± 0.8 1.2 ± 0.220:3x3 – – 0.1 ± 0.1 0.9 0.2 ± 0.6 0.2 ± 0.320:3x6 – – 7.6 ± 1.8 – 2.6 ± 3.7 –20:4x6 13.7 ± 2.8 8.9 ± 1.3 9.9 ± 4.9 11.2 10.3 ± 3.5 5.8 ± 1.220:5x3 6.9 ± 0.1 9.3 ± 2.2 9.3 ± 3.5 8.6 7.6 ± 0.4 12.3 ± 0.822:1x9 – 1.1 ± 1.0 0.9 ± 0.7 1.5 0.9 ± 0.2 0.8 ± 0.122:6x3 9.7 ± 2.8 19.7 ± 3.8 15.9 ± 2.9 17.5 15.5 ± 5.0 13.8 ± 1.324:1x6 5.9 ± 2.4 3.2 ± 1.9 2.4 ± 0.2 3.4 2.6 ± 0.2 1.8 ± 0.1P SFA 20.8 ± 4.7 32.1 ± 5.8 25.0 ± 4.4 21.3 20.6 ± 3.3 29.9 ± 4.5P MUFA 36.1 ± 3.9 27.6 ± 0.4 29.7 ± 5.2 15.3 25.4 ± 3.6 34.7 ± 2.2P PUFA 43.1 ± 8.5 40.4 ± 6.2 45.3 ± 9.5 34.2 41.2 ± 4.2 35.4 ± 3.9P planktonic 67.6 ± 3.7 59.4 ± 3.0 65.1 ± 3.8 67.0 67.4 ± 3.0 62.5 ± 4.2P bacterial 4.3 ± 2.9 5.7 ± 0.9 4.4 ± 1.4 – 3.5 ± 0.7 2.0 ± 0.416:1x7/16:0 0.3 ± 0.03 0.3 ± 0.1 0.4 ± 0.2 0.6 0.5 ± 1.4 0.6 ± 0.1Number of nematodes 300 300 313 ± 22 543 ± 11 300 300Nematodes dry weight (lg) 51.1 ± 25.4 87.0 ± 55.8 63.8 ± 21.9 121.5 ± 56 85.1 ± 42.1 112.9 ± 62.3FA concentrations (lg/350 lL extract) 0.6 ± 0.001 0.7 ± 0.1 1.4 ± 0.8 5.1 ± 3.5 1.4 ± 0.5 2.6 ± 1.3FA fractions (% of nematode dwt) 0.29 ± 0.03 0.63 ± 0.05 0.92 ± 0.6 6.21 ± 4.4 1.16 ± 0.4 3 ± 1.4Fig. 3. Principal Coordinates (PCO) plot based on the relative fatty acid composition of nematodes from all ANDEEP-SYSTCO stations. The vector overlay indicates FA-specificcorrelations of more than 60% with one to the first two PCO axes.

K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92 87Table 6Results from main and pairwise one-factor multivariate and univariate PERMANOVA and PERMDISP analyses testing for differences in nematode community composition, andnematode density, relative abundance, biomass, mean individual biomass, and juvenile/adult ratio (J/A), respectively, over the top 5 cm of the sediment between the sPF and sPF(2nd visit) station. Significant differences are indicated in bold.Test Factor NematodecommunityNematodedensityNematode relativeabundanceNematodebiomassNematode meanindividual biomassPERMANOVA Time df 1 1 1 1 1 1MS 2169.6 1.3 10 6b 3.4 10 12 559.2 a 7.9 10 4 0.13Pseudo-F 1.49 4.58 Denominator is 0 9.35 0.10 7.65Sediment depth df 4 4 4 4 4 4MS 3865.3 3781300 2439.8 1159.5 0.03 0.27Pseudo-F 3.66 b 33.61 b 53.43 b 27.48 b 3.14 a 3.57 aRe(Time) df 4 10 10 4 4 2MS 1456 287860 5.3 10 13 59.8 0.008 0.28Pseudo-F 1.38 a 2.56 a Negative 1.42 0.91 4.27 aTime x Sediment depth df 4 4 4 4 4 4MS 929.8 188480 192.0 202.0 0.002 0.054Pseudo-F 0.88 1.68 4.20 a 4.79 a 0.26 0.84Residuals df 16 40 40 16 16 8MS 1055.1 112510 45.66 42.19 0.009 0.07Total df 29 59 59 29 29 29PERMDISP Sediment depth F 0.49 0.05 0.41 8.89 a 0.007 1.97df 1 1 1 1 1 1 4df 2 8 8 8 8 8 25Pairwise test 0–1 cm: sPF, sPF (2nd visit) t 1.12 0.20 2.40 a 1.551–2 cm: sPF, sPF (2nd visit) t 0.91 2.15 1.05 0.322–3 cm: sPF, sPF (2nd visit) t 1.26 2.22 2.02 0.053–4 cm: sPF, sPF (2nd visit) t 0.92 1.28 0.13 0.164–5 cm: sPF, sPF (2nd visit) t 0.90 2.10 1.37 1.37a 0.001 < p 6 0.05.b p 6 0.001).Nematode J/ADespite the broad latitudinal range covered along the ANDEEP-SYSTCO transect (49–70° S, i.e. around 2400 km), relatively littlevariation is found between the deep-sea nematode communitiesin terms of generic composition. Although the MDS plot (Fig. 2)gives an indication of a subdivision into four communities, thelow percentage of exclusive genera at each station, together withthe dominance of the same four genera between all stations andmeiofauna-inherent, high small-scale variability within the stationscreates considerable overlap between most of the stations.It is more likely that identification to species level would reveala clearer separation in subcommunities, since a high degree ofspecies turnover between SO stations was found before (Vermeerenet al., 2004; Fonseca et al., 2006; Ingels et al., 2006; De Meselet al., 2006). The most remarkable community composition differenceamong the ANDEEP-SYSTCO stations is however the communityat the seamount Maud Rise (MR) which differs from all butthe abyssal south Polar Front (sPF) station. Similarly, the compositionof several macrofaunal groups at this station showed aclearly different composition from other formerly sampled stationsin the deep Weddell Sea (Brandt et al., 2011). Moreover,similar to the nematode assemblages, the composition of polychaetesat this seamount showed highest affinity to the sPF stations(Wilmsen and Schüller, 2011). The unique hydrographyregime at the seamount MR creates conditions that result in a differentfrequency, quantity and quality of fresh food compared toother Weddell Sea areas (Abelmann and Gersonde, 1991; Weferand Fischer, 1991). However, since MR is under influence fromseasonal sea-ice coverage, resulting in a lower organic carbon fluxwith a different composition compared to the Polar Front region(Wefer and Fischer, 1991), the ecological conditions that determinethe similarity between the nematode communities of theserelatively distant areas are unknown. The fauna at other seamounthabitats is, however, apparently often similar to neighboringareas that fall within organisms’ preferred depth ranges (Clarket al., 2010).The composition of the deep-sea nematode assemblages consideredat genus level along the ANDEEP-SYSTCO transect is comparablewith deep-sea nematode communities worldwide. Threeout of four genera that dominate at all ANDEEP-SYSTCO stations(Acantholaimus, Halalaimus, and Desmoscolex) are known as dominantgenera (>2% relative abundance) at deep-sea (i.e. slope to hadalzone) areas worldwide (Vanreusel et al., 2010). Our resultstherefore confirm that there is no distinct Antarctic nematodecommunity at genus level (Vanhove et al., 1999, 2004; Sebastianet al., 2007). In the study of Vanhove et al. (1999) nematode (generic)structural and trophic diversity decreased from the shelfbreak and upper slope (EG(100) = 40, H 1 = 3.85–3.45) towardsdown slope (EG(100) = 30, H 1 = 2.94). In comparison, the LazarevSea (LS) station at a comparable depth as the downslope station inthe Eastern Weddell Sea, has a higher structural and trophic diversity(EG(100) = 39, H 1 = 3.5). The rarefaction index for the LSslope station also agreed well with the index calculated for slopesworldwide (EG(100) = 40; Vanreusel et al., 2010.) Similarly to whatwas found on a worldwide scale, the rarefaction index reducedwhen the less diverse abyssal communities were taken into account(EG(100) = 34.5 versus 35.5 in Vanreusel et al. (2010)). TheLS station seemed to be the area of highest polychaete diversitytoo (Wilmsen and Schüller, 2011). Two factors that are generallybelieved to increase diversity at slopes compared to the abyss areenhanced food input and the reduced stability of the continentalslope environment due to the higher eventuality of landslides(Wilmsen and Schüller, 2011 and references therein).Epistratum feeders (2A) sensu Wieser (1953) dominated at moststations (LS, MR, sPF). Vanhove et al. (1995, 1999, 2004) and Sebastianet al. (2007) observed a dominance of epistratum feeders inSouthern Ocean slope and abyssal sediments where the highest inputof organic matter was expected based on highest nematodedensities. They explained this as a functional adaptation of nematodecommunities to short-term events of fresh food supply. However,no such link emerges when our feeding type compositions are

88 K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92compared with the labile portion of the carbon flux at each AN-DEEP-SYSTCO station, calculated by Sachs et al. (2009) (Table 1).4.2. Nematode fatty acid compositionsMost food web studies that investigate FA compositions of Antarcticmarine organisms focus on plankton (reviewed by Dalsgaardet al. (2003)). Although benthos is the richest element in the marinefood web in terms of numbers of species, their roles and interactionsare poorly known (Griffiths, 2010). Würzberg et al.(2011a,b) were the first to analyze the FA composition of membersof different Antarctic, benthic, polychaete families and orders ofperacarid crustaceans, in addition to their potential food sources,including sediment, bottom-water POM and foraminiferans. Thiswas done on samples collected at the same ANDEEP-SYSTCO stationsas the nematode samples for this study originated from.Moreover, the analyzed sediments originated from pseudo-replicatesamples, i.e. from the same multiple corer drops as the samplescollected to study the nematodes; thus allowing comparison.An indication for selective feeding behavior by nematodes isfound when comparing nematode FA patterns with FA data obtainedfor sediment and bottom-water POM from the stations sPF(2nd visit), cWS, MR and LS by Würzberg et al. (2011b). SFA(16:0, 18:0) and MUFA (16:1x7, 18:1x9, 18:1x7) dominated sedimentand bottom-water POM, while typical indicators of freshplanktonic detritus (PUFA; e.g. 20:5x3, 22:6x3) that occur in highproportions in nematodes (34–45%), were only detected in minorproportions in the sediment and bottom-water POM (9.4–28.7%and 9.1–19.2%, respectively, Table 7; Würzberg et al., 2011b). Thehigh portion of PUFAs in nematodes confirms that marine nematodescan be a high quality food source for predators (Leduc,2009). Nevertheless, the FA content of nematodes is relativelylow compared to e.g. marine zooplankton, i.e. minimum and maximumdiffering by one order of magnitude (Lee et al., 2006). Thisgenerally low FA content of the nematodes, together with the predominanceof typical phospholipids of biomembranes (20:5x3,22:6x3 and 16:0; Graeve et al., 1997) indicates that they do notaccumulate lipids for energy storage. This is in contrast with thestudy of Danovaro et al. (1999) who suggested that energy storageis a survival strategy of deep-sea nematodes based on their elevatedlipid concentrations compared to coastal nematodes. No increasein fatty acid content with depth appears along the ANDEEP-SYSTCO transect and the average fatty acid content in the Antarcticdeep-sea nematodes is considerably lower than in the Mediterraneandeep-sea nematodes (2% versus 17% of nematode dry weight,respectively). Whether the overall low fatty acid content of nematodesin this study is the result of low food availability or a constantfeeding behavior throughout the year is addressed furtherin the discussion based on the response to the seasonal food input.Overall, although FA profiles of polar lipids change with dietarycomposition (Peters et al., 2006), caution has to be taken wheninterpreting FA patterns of organisms with low lipid reserves. Sinceselective ingestion of fresh planktonic detritus cannot be distinguishedfrom strong retention of these highly unsaturated FA inmetabolic processes (Brett and Müller-Navarra, 1997) their proportionscould be enhanced (Würzberg et al., 2011b).A significant difference in nematode FA composition betweenthe southernmost slope station (LS) and all other stations wasfound. Furthermore, FA proportions of nematodes at the seamountMR differed from those at abyssal sPF (2nd visit) and PF stations.Since the pattern in FA compositions among stations is only weaklycorrelated with the pattern in nematode community compositions,the occurrence of distinct genera or distinct nematode feedinggroups (sensu Wieser, 1953) alone cannot explain the variance inFA compositions of the communities. We expect that the observedvariance in FA compositions can rather be explained by the combinationof variance in the FA composition of available food sourcesand the occurrence of distinct species with species-specific foodpreferences or metabolic characteristics resulting in different FAcompositions. The interpretation of FA as tracers of different foodsources is, however, complicated by many factors. Hydrodynamicprocesses in the first place, influence temperature, light and nutrientavailability, three key factors affecting the FA pattern of the localplanktonic primary producers (Dalsgaard et al., 2003). Waterdepth may also play a role, since lipid compositions of planktonand detritus can be altered considerably during sedimentationFig. 4. Nematode relative abundance (%) and total biomass (lg dwt per 10 cm 2 ) per centimeter from the south Polar Front station, before (black bars) and after (gray bars) thebloom settled. The averages and standard deviation of triplicates are plotted.Table 7Relative concentrations of saturated FA (SFA), monounsaturated FA (MUFA) and polyunsaturated (PUFA) in nematodes, sediment and bottom-water POM at the different ANDEEP-SYSTCO stations, based on data obtained in this study and the study of Würzberg et al. (2011b), respectively.PF sPF sPF (2nd visit) cWS MR LSNem Nem Nem Sed POM Nem Sed POM Nem Sed POM Nem Sed POMP SFA 20.8 32.1 25.0 35.1 47.9 21.3 25 58.9 20.6 31.2 62 29.9 30.9 45.4P MUFA 36.1 27.6 29.7 20.2 19 15.3 50.2 15.4 25.4 40.9 15.3 34.7 24.8 28.2P PUFA 43.1 40.4 45.3 11 11.3 34.2

K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92 89and after deposition due to catabolic processes and FA-specific diageneticsusceptibility (Graeve et al., 1997 and references therein;Camacho-Ibar et al., 2003 and references therein). In turn, diageneticalteration depends on environmental factors such as watertemperature and dissolved oxygen concentration (Camacho-Ibaret al., 2003 and references therein). The LS station is the shalloweststation, located closest to the shelf, where strong seasonality of icecoverageand of high carbon fluxes are reported (Bathmann et al.,1991; Fischer et al., 2000; Isla et al., 2009). Both sea-ice and pelagicblooms are largely composed of diatoms superimposed on a backgroundof Phaeocystis and dinoflagellates (Dalsgaard et al., 2003and references therein). Phaeocystis spp. in this region are muchless rich in x3-PUFA, which together with a low 16:1x7/16:0 ratioand an elevated concentration of 18:1x9 distinguishes them fromdiatoms (Skerratt et al., 1995). Our results indicate, however, thatboth 20:5x3 and 18:1x9 are high and the ratio of 16:1x7/16:0is low, suggesting a mixed diet including both diatoms and Phaeocystis,similar to what was found for the planktonic copepod Calanoidesacutus in the Lazarev Sea (Falk-Petersen et al., 1999). Ingeneral, however, it is impossible to say whether nematodes areprimary or secondary consumers of phytodetritus since zooplanktonmay incorporate FA markers from phytoplankton unchanged.The occurrence of 20:1x9 in nematodes along the ANDEEP-SYSTCOtransect might for example point towards the incorporation ofremnants of the Antarctic pelagic herbivorous copepods (e.g.Calanoides acutus and Calanus propinquus) that are known to biosynthesizethis MUFA de novo as storage product, while it is nota common phytoplankton FA (Hagen et al., 1993). Together withMetridia gerlachei, both copepod species accounted for >50% ofthe total zooplankton in stations along the Prime Meridian fromaround 50° southwards (Froneman et al., 2000). Results from severalsediment trap studies indicate that within the Marginal IceZone, copepods and krill may contribute substantially to totaldownward particle flux (Pakhomov et al., 2002 and referencestherein). Nevertheless, it is more generally accepted that outsidethe periods of sedimentation of ice-algae and phytoplanktonblooms, the sinking fecal material of zooplankton, that often containshigh concentrations of lipid droplets (Najdek et al., 1994) orundigested phytoplankton cells (Bathmann et al., 1991), largelydominates the downward vertical flux of POC (Pakhomov et al.,2002 and references therein). This may enable nematodes to feedyear-round as suggested by their relatively low FA content.What complicates the interpretation of FA patterns even more isto what extent typical FA are incorporated unmodified and the species-specificabilities to biosynthesize new FA. Knowledge on suchprocesses in the marine realm is limited to mostly crustaceous zooplanktonand fish (e.g. see Dalsgaard et al., 2003 for review), and sofar unknown for deep-sea benthic invertebrates. Furthermore, thespecificity of some conventional FA markers, as applied in this study,can be challenged. The proportion of 20:4x6, for example, is high innematodes at all stations. While it is generally considered to be aphytoplankton derived FA, it was also found in macroalgae, bacteria,copepods and deep-sea foraminiferans (Nichols et al., 1997; Russelland Nichols, 1999; Bühring et al., 2002; Gooday et al., 2002; Suhret al., 2003; Caramujo et al., 2008). Since it was however detectedin only very small proportions in two typical dominant herbivorouscopepods in the SO (Calanoides acutus and Metridia gerlachei, max.1.3 ± 0.8%; Albers et al., 1996), and in considerable proportions inforaminiferans at the ANDEEP-SYSTCO stations (max. 20.5 ± 8.4%;Würzberg et al., 2011a), the relatively high proportion found in nematodes(max. 13.7 ± 2.8%) might indicate feeding on foraminiferans,feeding on the food source where foraminiferans obtain this FA from,or partially by de novo biosynthesis. The latter is feasible since thepresence of D5 and D6 desaturase and x6 PUFA elongase activityin cultured nematodes (Caenorhabditis elegans and Panagrellus redivivus)has proven to result in de novo biosynthesis of 20:4x6(Wattsand Browse, 2002; Schlechtriem et al., 2004). Also the shallow waterfree-living nematode and bacterivore Rhabditis (Pellioditis) mediterraneashowed the ability to biosynthesize 20:3x6 and 20:4x6 whilecultured in a medium that did not contain these FA (Leduc and Probert,2009). Furthermore, both 20:5x3 and 22:6x3 are generally usedas biomarkers for phytoplankton since most marine organisms lackthe ability to synthesize them de novo. Several deep-sea bacteria,however, have shown the ability to produce these PUFA (e.g. Russelland Nichols, 1999; Nogi et al., 1998a,b; Nogi et al., 2002). Soalthough the small portion of conventional bacterial FA markers innematodes along the ANDEEP-SYSTCO transect (max 5.7%) suggeststhat bacteria are of minor importance to their diet, it is necessary todetermine the FA composition of bacteria sampled along the transectto validate this statement.4.3. Temporal variability at the south Polar FrontThe deposition of fresh phytodetritus at the abyssal sPF stationwas evidenced by the visual presence of a green fluffy layer, aneightfold increase in chlorophyll-a content in the first half centimetersediment layer and higher oxygen consumption due to enhancedrespiratory activity in the top centimeters, 52 days afterthe bloom was observed at the sea-surface (Veit-Köhler et al.,2011). In contrast to observations from subtidal North Sea sediments(Vanaverbeke et al., 2004), this event did not induce a rapidincrease in total nematode densities and biomass. Nevertheless,the occurrence of the genus Leptolaimus solely after the bloomhad settled and the significantly higher relative abundance in thetop centimeter at that time suggests that some changes are takingplace. Leptolaimus was demonstrated before to be a successfulearly colonizer of disturbed patches, including experimental phytodetritusdeposits (Ullberg and Ólafsson, 2003; Schratzbergeret al., 2004; Gallucci et al., 2008; Guilini et al., 2011). Its occurrencemight confirm the early stage of a succession process that is triggeredby the deposition of phytodetritus. Veit-Köhler et al.(2011) speculated that the higher relative abundance of meiofaunain the top centimeter indicates migration toward upper sedimentlayers due to the enhanced availability of organic material. If thelatter is true, then we expect to find evidence for uptake of freshorganic material in, for example, the total fatty acid content ofthe nematodes; which we did not find. Instead, the lack of a significantincrease in relative FA content (% of dry weight) in the nematodesafter the phytoplankton bloom had settled at the seafloorfavors the idea of a continuous feeding activity throughout theyear, which was also formulated by Würzberg et al. (2011a,b) forperacarid crustaceans and polychaetes originating from the sameANDEEP-SYSTCO stations based on their generally low total FAcontent (1.0–5.1% of individual dry weight, respectively). The ideathat meiofauna mainly feeds on degraded material is also supportedby the findings of Veit-Köhler et al. (2013) who report ononly small differences of carbon stable isotope composition amongsediment and meiofauna. The short-term response to the settledphytodetritus flux of nematodes inhabiting the sediment surfacelayer might, however, be underestimated considering a potentialdilution effect when pooling together nematodes from 5 cm sedimentprior to the FA analysis. Nevertheless, the reaction in termsof shifts in community structure or redistribution in the sedimentwas only weak and therefore points to an overall slow responsepossibly explained by the lack of an urge to feed at times of an excessof relatively fresh, labile, organic matter.5. ConclusionUnravelling the feeding ecology of deep-sea nematodes ismainly impeded by their small size which implies grouping a large

90 K. Guilini et al. / Progress in Oceanography 110 (2013) 80–92number of individuals to meet the biomass requirements for performingbiochemical analysis. Since culturing deep-sea nematodeshas been unsuccessful until now, FA analyses on species or genuslevel was restricted to communities where a single species dominates(Van Gaever et al., 2009). By combining analyses of communitystructure with fatty acid content and composition of deep-seanematodes in bulk, however, some interesting insights in theirfeeding ecology were gained, both on a latitudinal and a temporalscale. Nematode community composition was only weaklycorrelated with the community fatty acid composition, indicatingthat the occurrence of distinct genera or the proportion ofnematode feeding types sensu Wieser (1953) alone, cannot explainthe variance in FA compositions of the communities. Moreover, thegenerally low FA content of nematodes indicates that nematodesdo not have energy reserves and suggests that they may feedthroughout the year. A year-round foraging activity could alsoexplain the recorded lack of food uptake as a short-term responseto the recently settled phytodetritus at the Polar Front. Nevertheless,the higher relative abundance of nematodes in the topcentimeter layer of the sediment and the occurrence of the genusLeptolaimus only after phytodetritus had settled at the seafloor,suggests the recording of an early stage in the response to this seasonalevent.The lack of knowledge on the abilities of deep-sea nematodes tobiosynthesize FA de novo or to bioaccumulate unmodified FAimpedes to conclude which food sources nematodes actually use.Nevertheless, this study may serve as a base for comparison anddirective for future work. Comparative studies that include theFA analysis on both deep-sea nematodes and a spectrum ofpotential food sources have great potential to further elucidatethe deep-sea food web. Moreover, a differentiated analysis on theseparate feeding groups according to Wieser (1953) could help todetermine whether this commonly used classification has justified,practical implications for the role or functionality of deep-seanematodes.AcknowledgementsWe thank captain Uwe Pahl and his crew of RV Polarstern, thecruise leader Ulrich Bathmann and SYSTCO project leader AngelikaBrandt for their help and support during the ANT XXIV-2expedition. We acknowledge Annika Hellmann who was incharge of the SYSTCO-logistics and the multicorer deploymentson board, Marco Bruhn who coordinated sample treatment andsorted the meiofauna, and Katharina Bruch and Daniela Hugowho helped with sample processing. Niels Viaene and AnnickVan Kenhove are also greatly acknowledged for their help withglass slide preparation and nematode measurements. We thankthe Flanders Marine Institute (VLIZ), in particular Nathalie DeHauwere, for generating the bathymetric maps. The Census ofMarine Life projects CeDAMar and CAML as well as Senckenbergam Meer – DZMB are thanked for financial and logistical supportof the SYSTCO-team. This study was realised with the financialsupport of the Research Foundation – Flanders (FWO, projectnumber 3G0346), the Special Research Fund (BOF, The relationbetween FUNction and biodiversity of Nematoda in the DEEPsea(FUNDEEP), project number 01J14909), the Belgian SciencePolicy (Belspo, Biodiversity of three representative groups ofthe Antarctic Zoobenthos – Coping with Change (BIANZO II), researchproject SD/BA/02A), Ghent University (BOF-GOA01GA1911W), and the Friedrich Wilhelm and Elise Marx Foundation.We also thank the three anonymous referees for their detailedand constructive feedback. This is ANDEEP-SYSTCOpublication # 176.ReferencesAbdulkadir, S., Tsuchiya, M., 2008. One-step method for quantitative and qualitativeanalysis of fatty acids in marine animal samples. Journal of ExperimentalMarine Biology and Ecology 354, 1–8.Abelmann, A., Gersonde, R., 1991. 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