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

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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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