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Trophic structure on the West Antarctic Peninsula shelf: Detritivory andbenthic inertia revealed by d13C and d15N analysis

Sarah L. Mincks a,�, Craig R. Smith b, Rachel M. Jeffreys c, Paulo Y.G. Sumida d

a University of Alaska, School of Fisheries and Ocean Sciences, PO Box 757220, Fairbanks, AK 99775, USAb Department of Oceanography, University of Hawai’i, 1000 Pope Road, Honolulu, HI 96822-2225, USAc Royal Netherlands Institute for Sea Research, PO Box 59, Den Burg, Texel, 1790 AB, The Netherlandsd Oceanographic Institute, University of Sao Paulo, Prac-a do Oceanografico, 191, Sao Paulo-SP 05508-120, Brazil

a r t i c l e i n f o

Article history:

Accepted 30 June 2008Available online 31 July 2008

Keywords:

Stable isotopes

Benthos

Antarctic shelf

Food webs

Benthic–pelagic coupling

Deposit feeding

a b s t r a c t

Summer bloom-derived phytodetritus settles rapidly to the seafloor on the West Antarctic Peninsula

(WAP) continental shelf, where it appears to degrade relatively slowly, forming a sediment ‘‘food bank’’

for benthic detritivores. We used stable carbon and nitrogen isotopes to examine sources and sinks of

particulate organic material (POM) reaching the WAP shelf benthos (550–625 m depths), and to explore

trophic linkages among the most abundant benthic megafauna. We measured d13C and d15N values in

major megafaunal taxa (n ¼ 26) and potential food sources, including suspended and sinking POM, ice

algae, sediment organic carbon, phytodetritus, and macrofaunal polychaetes. The range in d13C values

(414%) of suspended POM was considerably broader than in sedimentary POC, where little temporal

variability in stable isotope signatures was observed. While benthic megafauna also exhibited a broad

range of d13C values, organic carbon entering the benthic food web appeared to be derived primarily

from phytoplankton production, with little input from ice algae. One group of organisms, primarily

deposit-feeders, appeared to rely on fresh phytodetritus recovered from the sediments, and sediment

organic material that had been reworked by sediment microbes. A second group of animals, including

many mobile invertebrate and fish predators, appeared to utilize epibenthic or pelagic food resources

such as zooplankton. One surface-deposit-feeding holothurian (Protelpidia murrayi) exhibited seasonal

variability in stable isotope values of body tissue, while other surface- and subsurface-deposit-feeders

showed no evidence of seasonal variability in food source or trophic position. Detritus from

phytoplankton blooms appears to be the primary source of organic material for the detritivorous

benthos; however, seasonal variability in the supply of this material is not mirrored in the sediments,

and only to a minor degree in the benthic fauna. This pattern suggests substantial inertia in

benthic–pelagic coupling, whereby the sediment ecosystem integrates long-term variability in

production processes in the water column above.

Published by Elsevier Ltd.

1. Introduction

The West Antarctic Peninsula (WAP) shelf is subject to highlyseasonal deposition of particulate organic carbon (POC), derivedfrom large summer phytoplankton blooms in December–Marchfollowing the retreat of winter sea-ice (e.g., Karl et al., 1996; Smithet al., 1996; Ducklow et al., 2006). Major contributors toparticulate flux could include ice algae released from meltingsea-ice and pelagic phytoplankton released from light-limitationas the ice edge retreats. Sediment-trap data from the Antarcticcontinental shelf indicate that summer particle fluxes can be

orders of magnitude larger than in ice-covered winter months(Wefer et al., 1988; Dunbar et al., 1989; Honjo, 1990). Bloom-derived particulates are large and fast sinking, and may reach theseabed with relatively minimal degradation (Honjo, 1990; Karlet al., 1996; Nelson et al., 1996). Thus, these summer detrituspulses represent the primary input of organic material to benthiccommunities on the WAP shelf (Smith et al., 2006, 2008).

Seasonal phytodetrital pulses are known to induce temporalvariability in benthic ecological processes and carbon cycling inmany regions (Grebmeier et al., 1988; Grebmeier and McRoy,1989; Gooday and Turley, 1990; Ambrose and Renaud, 1995;Pfannkuche et al., 1999; Beaulieu, 2002). However, in WAP shelfsediments, food availability exhibits much less seasonality than inthe overlying water column (Gutt, 2000; Mincks et al., 2005)because sediments appear to store labile organic material on time

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Deep-Sea Research II

0967-0645/$ - see front matter Published by Elsevier Ltd.

doi:10.1016/j.dsr2.2008.06.009

� Corresponding author. Tel.: +19074747616; fax: +19074747204.

E-mail address: mincks@sfos.uaf.edu (S.L. Mincks).

Deep-Sea Research II 55 (2008) 2502–2514

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scales of months to years, forming a persistent sediment ‘‘foodbank’’ for benthic detritivores (Mincks et al., 2005; Smith et al.,2006, 2008).

Abundance and biomass of benthic organisms on the Antarcticcontinental shelf and slope are typically high compared to othershelf and deep-sea environments (Arntz et al., 1994; Brey andGerdes, 1997; Glover et al., 2008). Thus, detritivore feeding onbloom-derived material could have a large impact on the quantityand quality of organic material ultimately buried in the sedi-ments. Feeding activities and trophic relationships of benthicfauna must be evaluated to determine the fate of bloom materialreaching the seafloor. Studies of food web structure, whichhistorically relied on gut-content analyses, are increasinglyemploying stable isotope techniques (e.g., Hobson and Welch,1992; Iken et al., 2001). However, very few such studies have beenperformed in Antarctic benthic communities (but see Kaehleret al., 2000; Dunton, 2001; Nyssen et al., 2002).

The stable isotopic signature of an organism’s tissues isgenerally related to its food source. On average, consumers areenriched relative to food material (the so-called ‘‘trophic shift’’) byabout 3–5% in d15N, and by o1% in d13C (DeNiro and Epstein,1978, 1981; Minagawa and Wada, 1984; Peterson and Fry, 1987;Michener and Schell, 1994). The smaller fractionation of d13Cmakes it useful for distinguishing food sources with distinctlydifferent d13C signatures, whereas d15N is better suited todelineating trophic levels (Peterson and Fry, 1987; Hobson andWelch, 1992). Stable isotope analysis is particularly useful fortrophic studies of deposit-feeders, in which sources of ingestedorganic material are difficult to identify visually (Hentschel, 1998).Further, since the method measures material incorporated into anorganism’s tissues, it provides a time-averaged indication ofmaterial actually assimilated by the organism, rather than asnapshot of the material consumed at a particular point in timeand space.

We used stable isotope techniques to examine sources andsinks of POC reaching the WAP shelf sediments. Previousobservations of a sediment food bank on the WAP shelf(Mincks et al., 2005; Smith et al., 2006) led us to predict littletemporal variability in stable isotope values of the benthos,despite extreme annual/interannual variability in particu-late organic-carbon flux (e.g., Ducklow et al., 2006). By measuringstable isotope ratios in dominant benthic megafauna andpotential food sources, we examined (1) temporal patternsin the source and quality of organic material depositedin sediments, (2) trophic relationships within the benthiccommunity, and (3) temporal variability in nutritional resourcesfor benthos.

2. Methods

Samples were collected on the five 22-d FOODBANCS cruises tothe WAP continental shelf (Smith et al., 2008). To evaluateseasonal and interannual variability in POC flux and benthicecosystem response, these cruises were conducted over a16-month period, occurring in (I) Nov–Dec 1999 (early summer-bloom season), (II) Mar 2000 (end of the summer bloom), (III) Jun2000 (winter oligotrophic period), (IV) Oct 2000 (end ofwinter, during winter sea-ice retreat) and (V) Feb–Mar 2001(second summer bloom). Three stations (A, B, and C) weresampled along a transect crossing the continental shelf nearAnvers Island (Fig. 1). Water depth was 550–650 m at all stationssampled. Sonar and photographic surveys (C. Smith et al.,unpublished data; Smith et al., 2008; Sumida et al., 2008)revealed little topographic relief at Stations B and C. However,Station A was located in a basin approximately 25 km wide, sotopographic focusing could have impacted sediment processes inthis area.

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Fig. 1. Map of the study area. (K) Locations of Stations A, B and C; (.ST) Location of sediment trap mooring. Depth contours are in m.

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2.1. Sample collection and analysis

Surface plankton samples were collected using a 30-cm ringnet (20mm mesh). Oblique plankton tows were also conductedfrom the surface to within 20–50 m of the seafloor using a TuckerTrawl (80mm mesh). Plankton samples were frozen in bulk,without removal of zooplankton. Ice algae were collected onCruise I (Nov 1999) and Cruise IV (Oct 2000) by melting pieces ofsea ice at room temperature. Particulate material was collectedafter settling out of the melt water. Sinking particulate organicmaterial (POM) was collected in two replicate, single-cupsediment traps (c.f., Dunbar et al., 1989; mouth opening0.159 m2) deployed on a single mooring at 150 and 170 m abovebottom, in the vicinity of Station B (Fig. 1, ‘‘ST’’). Traps wereemptied and re-deployed on each cruise (i.e., at 90–120-dintervals) until final recovery in Mar 2001. Trap contents werepreserved in situ in hypersaline formalin solution (5% NaCl wt/wt,10% formalin vol/vol) and kept refrigerated. Swimmers such aspelagic copepods and krill were removed under microscopicexamination. Suspended and sinking particulates from nets andtraps were freeze-dried prior to stable isotope analysis.

Sediment cores (10 cm diameter) were collected on everycruise, from each of at least five randomly located deploymentsper station, using a Bowers & Connelly Megacore. Surface(0–0.5 cm) and subsurface (4–6 cm) sediment samples werecollected and stored at �20 1C for stable isotope analysis. Whena phytodetritus layer (greenish flocculent material includingintact phytoplankton cells) was visible at the surface of a core(Cruise V only), it was removed with a large syringe and handledseparately. Sediments and phytodetritus were freeze-dried priorto analysis.

Benthic fauna were collected using a 5.5 m semi-balloon ottertrawl (2 cm mesh; one to three trawls collected per station percruise). Abundant taxa were selected for food web analysis. Thesetaxa, including representatives from eight phyla, were classifiedinto four trophic groups based on morphology and conclusionsfrom published literature. Up to 10 individuals of each taxon wereindividually sealed in plastic bags, and flash-frozen in liquid N2.All animals were stored at p�20 1C. The dominant macrofaunalorganism, the polychaete Aurospio sp. n. with densities of roughly8000 m�2 (Glover et al., 2008), was collected from formalin-preserved sediment cores sieved on 300mm mesh and analyzed asa potential megafaunal food source. Due to their small size,Aurospio were analyzed whole, with 10–15 individuals pooledtogether for each measurement.

Target tissues were removed from frozen megafauna, withgreat care taken to minimize tissue warming. All animal tissuesamples were then dried at 60 1C and ground by hand with amortar and pestle. In general, we analyzed body wall or muscletissue; however, to obtain adequate tissue masses, we used wholeasteroid arm pieces, whole pycnogonid legs, ligament from theAristotle’s lantern of the regular echinoids, and gonad from theirregular echinoids. Calcareous animal tissues (e.g., asteroid armpieces) and trophic end-members (e.g., sediments, plankton) wereacidified with 10% HCl to remove carbonates, which can bias d13Csignatures (c.f., McConnaughey and McRoy, 1979; Hobson andWelch, 1992; Jacob et al., 2005).

Stable isotope analyses were performed at the University ofHawai’i at Manoa, SOEST mass spectrometer facility. Isotope ratiosare expressed as parts per thousand (%) differences from standardreference material according to the following equation:

dX ¼ ½ðRsample=RstandardÞ � 1� � 1000

where X is 13C or 15N and R is the corresponding ratio 13C/12Cor 15N/14N. Rstandard for 13C and 15N are from PeeDee Belemnite(PDB) and atmospheric N2, respectively. A reference material,

cicloesanone, was analyzed approximately every eight samples,indicating analytical errors of 70.12% and 0.2% for C and N,respectively.

Formalin preservation could not be avoided in samples fromsediment traps deployed continuously for 3–4-month periods. Inaddition, macrofaunal polychaetes were only available at the timeof analysis from formalin-preserved sediment cores. We tested theeffects of formalin preservation on stable isotope values of animaltissues in four species of megafauna, and found only small,statistically insignificant differences in d13C (D ¼ 0.08–0.94%) ord15N (D ¼ 0.73–1.26%) between frozen and formalin-preservedtissues from the same organisms. Other authors also report small(�1%) decreases in d13C (Rau et al., 1982; Bosley and Wainright,1999; Kaehler and Pakhomov, 2001; Sarakinos et al., 2002), and0–1.4% increases in d15N (Bosley and Wainright, 1999; Kaehlerand Pakhomov, 2001) with formalin preservation. We reportsediment-trap POM and polychaete data with the caveat that d13Cvalues may only be accurate within a range of 71%, and d15Nvalues within a range of 71.5%. However, given the relativelylarge differences in d13C signatures of potential food sources(e.g., Table 1) and expected trophic shifts in d15N, any formalinpreservation effects have had little impact on our interpretationsof stable isotope data.

2.3. Data analysis

Statistical analyses were conducted using Statistical Packagefor the Social Sciences (SPSS) software. We tested differences instable isotopic signature of sediments across time and space(i.e., time and station effects, and time–station interaction) usingmultivariate ANOVA. One-way ANOVA was used to test temporaldifferences at each particular station, with post hoc tests (leastsignificant difference) indicating differences between specifictime points. Net-collected plankton samples from all threestations were pooled together due to low numbers of samples(n ¼ 1) per station, and temporal variability in isotopic composi-tion was tested using one-way ANOVA. Similarly, sediment-trapmaterial was only collected at one station, and thus one-wayANOVA was applied to test temporal variability. In cases wherethe assumption of homogeneity of variances could not be met, weapplied the non-parametric Kruskal–Wallis test. Five benthic taxarepresenting various trophic groups were also tested for temporaldifferences in stable isotope values. Organisms were primarilysampled from a single station, so data were pooled to test only fora temporal effect using one-way ANOVAs as above. An a level of0.05 was used as the criterion for statistical significance.

3. Results

3.1. Trophic end-members

Stable isotope data and C:N ratios for all organic sourcematerials are summarized in Table 1, with temporal differences insinking and suspended POM and sediments shown in Fig. 2. Net-collected plankton exhibited substantial temporal and spatialvariability in d13C (�20% range), but very little variability in d15N(Fig. 2). However, despite the wide range in d13C values, temporaldifferences were not quite statistically significant (p ¼ 0.095),probably due to differences between stations at each time pointresulting in large variances (Fig. 2, see especially Mar 2001).Differences in d13C of net plankton between the two summerseasons (Mar 2000 and Mar 2001), were sizeable although notstatistically significant (Fig. 2), and coincided with the changes inthe dominant species of pelagic diatom collected. d15N did notvary significantly across time, despite much smaller variances.

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Stable isotope analyses were performed on the bulk planktonsamples, so seasonal differences in isotopic composition of theplankton may reflect relative changes in zooplankton abundance(especially krill larvae and juveniles), as well as seasonalvariations in phytoplankton biomass. Microscopic examinationof fresh and formalin-preserved plankton samples indicated verylow abundance of large phytoplankton in Nov 1999, whereas thecentric diatom Corethron criophilum was very abundant inMar 2000. Winter net tows (Jun 2000) were composed mainlyof juvenile krill and salps. The following spring (Oct 2000),C. criophilum was again abundant in plankton samples from allstations. By summer (Mar 2001), a different suite of diatoms hadappeared, with Coscinodiscus cf., bouvet dominating at Station A,Rhizosolenia sp. dominating at Station C, and a mixture of bothtypes occurring at Station B. All three of these taxa representtypical components of the pelagic bloom-forming algal commu-nity in Antarctic coastal waters, which is often dominated bycolonial diatoms (e.g., Priddle, 1990).

Particulate material collected in sediment traps varied sig-nificantly across time in both d13C and d15N (p ¼ 0.003 and 0.026,

respectively), although the range in isotopic values was muchnarrower for trap material than for net plankton (Fig. 2). Post hoc

tests indicate that spring and summer samples within one bloomperiod (i.e., collections from Cruises II and III or Cruises IV and V)did not vary significantly in d13C, whereas values did varysignificantly (42%) between the two years (Cruises II and V;p ¼ 0.003; Fig. 2). d13C values of sediment-trap material collectedfrom Nov 1999 to Jun 2000 resembled that of net plankton fromMar 2000 (Fig. 2), suggesting that the bulk of material in the trapswas deposited during the summer phytoplankton bloom. How-ever, microscopic examination indicated that the large input ofmaterial that had reached sediment traps by Mar 2001 wascomprised of different diatoms (Corethron criophilum) than thosepresent in the overlying surface waters at that time (Coscinodiscus

and Rhizosolenia spp.). Significant differences in d15N of sinkingPOM were only observed between the winter collection(Jun 2000–Oct 2000) and all other time points. The d15N valueof the winter trap material was only about 1% higher thanplankton, but about 3.5% higher than trap material collected inother months (Table 1, Fig. 2). Heavier d15N values during winter

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Table 1Mean stable isotope values (%) and C:N ratios (wt/wt) of particulate organic matter and sediments

Source material Cruise Station N d13C d15N C/N

Ice algae I A 1 �19.02 6.0 7.3

IV B 1 �19.48 4.5 4.7

Plankton I B 1 �27.18 3.7 6.3

C 2 �33.93 (0.15) 4.3 (1.5) 4.8 (0.2)

II A 1 �33.14 5.3 4.1

B 1 �31.32 5.6 5.5

C 1 �26.08 4.6 4.4

III A 1 �25.70 4.3 4.0

B 1 �26.88 5.0 5.0

C 1 �27.30 6.6 4.9

IV A 1 �28.85 3.3 4.9

B 1 �25.83 7.5 4.0

C 2 �29.56 (3.44) 4.2 (2.4) 4.5 (0.2)

V A 1 �14.94 6.8 5.4

B 1 �18.45 4.2 3.6

C 1 �29.91 3.2 4.9

Phytodetritus V A 2 �22.92 (0.22) 6.2 (0.2) 5.9 (0.6)

B 2 �25.73 (0.09) 5.7 (0.3) 6.2 (0.03)

C 1 �25.46 7.9 5.7

Sediment trap II B 2 �30.19 (0.17) 1.8 (0.09) 5.8 (0.1)

III B 2 �29.58 (0.49) 3.4 (0.2) 6.2 (0.02)

IV B 2 �26.80 (0.04) 5.9 (1.1) 5.2 (0.1)

V B 2 �27.67 (0.20) 3.1 (0.06) 6.7 (0.1)

Surface sediments (0–0.5 cm) I A 2 �24.05 (0.03) 4.1 (0.01) 6.8 (0.1)

B 2 �26.61 (1.63) 4.6 (0.2) 7.4 (0.7)

C 2 �25.93 (0.57) 4.2 (0.1) 6.8 (0.2)

II A 2 �24.38 (0.04) 3.7 (0.2) 6.8 (0.05)

B 2 �25.03 (0.10) 4.2 (0.2) 6.7 (0.1)

C 2 �25.29 (0.23) 3.9 (0.5) 6.7 (0.01)

III A 2 �24.00 (0.05) 4.3 (0.1) 7.0 (0.05)

C 2 �25.18 (0.09) 3.6 (0.8) 6.5 (0.06)

IV A 2 �24.62 (1.11) 2.8 (0.7) 6.7 (0.2)

C 2 �25.11 (0.02) 4.3 (0.09) 6.6 (0.06)

V A 2 �24.15 (0.22) 6.4 (0.5) 6.3 (0.2)

B 2 �25.77 (0.42) 4.6 (1.1) 6.1 (0.3)

C 1 �25.05 5.6 6.0

Subsurface sediments (4–6 cm) II A 1 �23.69 5.0 7.2

B 1 �25.00 6.2 7.0

C 1 �25.36 8.1 6.4

V A 2 �23.40 (0.03) 6.1 (0.4) 6.3 (0.1)

B 2 �24.88 (0.03) 6.3 (0.6) 6.2 (0.2)

C 1 �25.08 6.0 6.3

Standard errors, where applicable, are indicated in parentheses. Cruise(s) and Station(s) indicate time and place of collection for all samples included in the mean. Cruise

I ¼ Nov 1999, II ¼Mar 2000, III ¼ Jun 2000, IV ¼ Oct 2000, V ¼Mar 2001.

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months suggest settling of reworked organic material suchas krill fecal strings and exuviae and laterally advected sedi-ments (Smith et al., 2006) following the cessation of the summerbloom.

The range in d13C values was narrower for sediment trap thanfor plankton samples, and narrower still for surface sediments(Table 1, Fig. 2). In general, surface sediments were slightlyheavier in both d13C and d15N than sediment-trap material,indicating dilution by a pool of more refractory material at theseafloor and/or additional transformation of organic material inthe water column below trap depths. A significant spatialdifference was detected for d13C (p ¼ 0.013), and a temporaldifference for d15N (p ¼ 0.012) in surface sediments, but thespace–time interaction effect was not significant. Station A surfacesediments were heavier in d13C (2%) than the other stations(Table 1, Fig. 2). d15N values varied temporally only at Station A,with lower values in Oct 2000, and higher values in Mar 2001than in other months. Subsurface sediments (4–6 cm depth) wereonly analyzed from the two summer sampling periods (Mar 2000and Mar 2001), and both d13C and d15N varied little between years(Table 1). d13C values of subsurface sediments roughly matchedthose of surface sediment, whereas d15N values were in somecases heavier than surface sediments by up to 4% (Table 1).

d13C of phytodetritus (Mar 2001 only) fell mid-way betweenOct 2000 and Mar 2001 net plankton (Table 1), indicatingderivation from summer phytoplankton-bloom material. d15Nenrichment in phytodetritus relative to plankton was onlyobserved at the more northerly Station C, where ice-cover islikely to have disappeared first, and bloom material to havesettled out earlier in the season. At Station A, phytodetritusmatched surface sediments in d15N, but was 1% enriched in d13C.

In contrast, Stations B and C phytodetritus was 1–2% enriched ind15N, but equivalent to surface sediment in d13C value (Table 1).

3.2. Benthic fauna

Mean stable isotope values for megafaunal tissues aresummarized in Table 2 and Fig. 3. For descriptive purposes,predators and scavengers (P/S) are qualitatively grouped into twogeneral categories (Fig. 3). P/S I includes low-mobility and/orsessile fauna, such as gastropods, asteroids, and anemones. P/S IIincludes larger, more mobile epibenthic foragers and scavengerssuch as fish, octopus, and giant scale worms. We observed a broadrange in d13C values, from about �27% to �17%. In contrast, allbut two species fell within a 4% range in d15N. Given averagetrophic shifts of about 3.5% for d15N (Rau et al., 1983; Michenerand Schell, 1994), this small range in d15N values suggests thatmost of the sampled animals, including predatory fish andoctopus, occupy approximately two trophic levels. Based ontrophic-shift assumptions, a standard predatory food chain shouldhave a slope of �3.5 on a plot of d13C versus d15N. The slope of thed13C versus d15N relationship in our study is much lower, withhighly mobile demersal predators (fish) falling along a line with aslope of �1.5 (R2

¼ 0.807).Deposit feeders and invertebrate predators and scavengers are

very broadly distributed in d13C and d15N space (Figs. 3 and 4).Two organisms, the sponge Cinachyra antarctica and the pencilurchin Ctenocidaris perrieri, exhibited unusually high d15N signa-tures, but fell within the same d13C range as the other organisms.To identify potential food sources, trophic-shift boxes enclosingthe expected ranges of enrichment in d13C and d15N (0–1% and3–5%, respectively) from feeding on a particular food source are

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Net-Collected Plankton

Station AStation BStation Cmean

Sedimenting POM and Surface Sediments

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-12Station A surf sedStation B surf sedStation C surf sedmean surf sedSediment Traps

0

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Fig. 2. d13C (top panels) and d15N (bottom panels) values for net-collected plankton (left side), surface sediments and sediment traps (right side) across time. Individual

station values are indicated by open symbols for net plankton and surface sediment, and means of all three stations 71 standard error are indicated with solid circles.

Values for sediment traps represent the mean (71 standard error) of top and bottom traps, deployed on a single mooring at Station B.

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plotted in Fig. 4. Surface-deposit-feeders (SDFs) generally fall intothe trophic-shift boxes for ‘‘sediment-trap material’’ and ‘‘surfacesediments’’. In contrast, subsurface-deposit-feeders (SSDFs) fitpoorly into the ‘‘subsurface sediments’’ box, exhibiting a muchwider range than expected in d13C values.

Five taxa were examined for temporal variability in stableisotope signatures (Fig. 5), including the surface-deposit-feedingholothurians Peniagone vignoni and Protelpidia murrayi andmacrofaunal polychaetes Aurospio sp. n., the suspension-feedingcrinoid Promachocrinus kerguelensis, and the bivalve Limopsis

marionensis. Significant temporal variability was detected only inthe holothurians and the crinoid. P. vignoni (Fig. 5A) showed

significant temporal variation in d15N (F ¼ 5.224, p ¼ 0.014), withno significant differences in d13C. Post hoc comparisons for d15Nrevealed significant differences between Mar 2001 and all othertime points (Table 3). P. murrayi (Fig. 5B) exhibited much moretemporal variability than P. vignoni, with significant differences inboth d13C (F ¼ 7.199, p ¼ 0.006) and d15N (F ¼ 10.576, p ¼ 0.001).Post hoc comparisons indicate variation both within and betweenbloom periods (Table 3). P. kerguelensis (Fig. 5C) varied signifi-cantly across time in d15N (F ¼ 7.757, p ¼ 0.009), but variation ind13C was not quite significant (p ¼ 0.072) (Table 3). d15N differedbetween winter and spring (Jun and Oct), and between winter andsummer (Jun and Mar) in the 2000/2001 bloom season (Table 3).

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Table 2Mean stable isotope values (%) and C/N ratios of benthic invertebrates and fish

Species Feeding type Ni d13C d15N C/N

Echinodermata

Holothuroidea

Peniagone vignoni SDF 17 �24.45 (0.20) 8.2 (0.2) 3.5 (0.1)

Protelpidia murrayi SDF 15 �23.54 (0.32) 8.0 (0.2) 3.6 (0.09)

Molpadia musculus SSDF 5 �18.35 (0.87) 10.2 (0.2) 4.8 (0.2)

Ypsilocucumis turricata SSDF 4 �18.88 (0.28) 10.5 (0.5) 4.1 (0.2)

Pseudostichopus mollis SDF 5 �24.22 (0.16) 10.0 (0.3) 3.7 (0.2)

Asteroidea

Bathybiaster loripes obesus P/S 5 �22.65 (0.38) 9.2 (0.5) 3.4 (0.1)

Cuenotaster involutus P/S 5 �22.51 (0.48) 9.9 (0.3) 3.5 (0.04)

Echinoidea

Amphipneustes lorioli SSDF 5 �25.99 (0.17) 8.6 (0.2) 6.8 (0.6)

Amphipneustes rostratus SSDF 5 �27.16 (0.54) 8.0 (0.3) 7.3 (0.6)

Ctenocidaris perrieri P/S 5 �21.46 (0.16) 15.6 (0.2) 3.4 (0.6)

Sterechinus antarcticus P/S 5 �23.60 (0.22) 10.2 (0.3) 2.8 (0.5)

Crinoidea

Promachocrinus kerguelensis SF 12 �25.70 (0.26) 8.4 (0.2) 4.2 (0.1)

Mollusca

Bivalvia

Limopsis marionensis SF? 14 �21.87 (0.12) 10.1 (0.09) 3.3 (0.03)

Gastropoda

Aforia magnifica P/S 4 �21.28 (0.41) 9.5 (0.4) 3.9 (0.1)

Harpovoluta charcoti P/S 5 �20.62 (0.65) 10.6 (0.2) 3.7 (0.08)

Cephalopoda

Pareledone sp. P/S 7 �24.50 (0.12) 9.1 (0.3) 3.9 (0.6)

Arthropoda

Pycnogonida

Colossendeis sp. P/S 5 �25.98 (0.18) 7.3 (0.4) 4.0 (0.08)

Amphipoda

Natatolana meridionalis P/S 4 �23.91 (0.99) 8.0 (0.7) 4.7 (0.2)

Cnidaria

Anthozoa

Hormathia lacunifera P/S 4 �22.16 (0.22) 8.9 (0.2) 3.1 (0.3)

Isosycionis alba P/S 5 �26.52 (0.51) 8.3 (0.4) 4.5 (0.2)

Annelida

Polychaeta

Laetmonice producta P/S 4 �23.60 (0.78) 11.4 (0.7) 3.6 (0.2)

Aurospio sp. n. SDF 12 �24.98 (0.04) 7.9 (0.06) 3.6 (0.1)

Echiuria

Bonellidae sp.indet. SDF 4 �21.27 (1.10) 10.2 (0.6) 3.3 (0.1)

Porifera

Cinachyra antarctica SF 4 �21.63 (0.53) 16.5 (0.2) 3.9 (0.1)

Vertebrata

Osteichthys

Lycodichthys sp. (eelpouts) P/S 5 �24.23 (0.53) 10.6 (0.7) 3.5 (0.1)

Nototheniid sp. P/S 5 �24.86 (0.30) 10.7 (0.3) 3.5 (0.09)

Chionodraco rastrospinosus (ice fish) P/S 5 �25.88 (0.12) 7.6 (0.2) 3.4 (0.05)

Feeding type abbreviations refer to surface-deposit-feeders (SDF), subsurface-deposit-feeders (SSDF), suspension feeders (SF), and predators/scavengers (P/S). Numbers in

parentheses ¼71 standard error. Ni ¼ number of individuals.

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4. Discussion

4.1. Seasonal bloom dynamics and deposition of organic

material in sediments

The spatial and temporal variability in d13C of net-collectedplankton provides additional evidence of variability in summer-

bloom dynamics previously described for FOODBANCS and otherWAP shelf sites (e.g., Smith et al., 2008; Ducklow et al., 2006). Lightd13C values (o�30%) detected in spring and summer are typical ofSouthern Ocean phytoplankton communities (e.g., Wada et al.,1987; Fischer, 1991; Rau et al., 1991b; Nyssen et al., 2002), in whichslow, light-limited growth in the presence of high CO2(aq)

concentrations promotes strong carbon fractionation and unusually

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Pseudostichopus

asteroids

bivalve

pycnogonid

irregular urchins

Sterechinus

octopusI. alba

scale worm

crinoid

echiurian

eelpout

Nototheniid

ice fishamphipod

Aurospio sp. n.

Surface SedimentPlankton4

6

8

10

12

14

16

18

-28

δ13C

δ15N

P/S I

P/S II

Ctenocidaris perrieri

Molpadia musculus

sponge

Ypsilocucumis turricata

Protelpidia murrayi

Hormathia lacunifera

Aforia magnifica

Peniagone vignoni

Harpovoluta charcoti

-26 -24 -22 -20 -18 -16

Fig. 3. Mean stable isotope values (d13C versus d15N) for benthic fauna, with average surface sediment and net plankton values. Points represent overall means, including all

stations and cruises. Symbols refer to feeding type (K ¼ Predators/Scavengers; ’ ¼ Subsurface Deposit Feeders; & ¼ Surface Deposit Feeders; B ¼ Suspension Feeders).

Ovals labeled P/S I and P/S II indicate members of predator/scavenger groups I and II (see Results, Section 3.2). Error bars indicate 71 standard error, n ¼ 4 to 13. Non-

specific labels are as follows: ‘‘irregular urchins’’ ¼ Amphipneustes lorioli and A. rostratus; ‘‘asteroids’’ ¼ Bathybiaster loripes and Cuenotaster involutus; ‘‘sponge’’ ¼ Cinachyra

antarctica; ‘‘pycnogonid’’ ¼ Colossendeis sp.; ‘‘ice fish’’ ¼ Chionodraco rastrospiosus; ‘‘I. alba’’ ¼ Isosycionis alba; ‘‘bivalve’’ ¼ Limopsis marionensis; ‘‘scale worm’’ ¼ Laetmonice

producta; ‘‘amphipod’’ ¼ Natatolana meridionalis; ‘‘octopus’’ ¼ Pareledone sp.; ‘‘crinoid’’ ¼ Promachocrinus kerguelensis; ‘‘Sterechinus’’ ¼ Sterechinus antarcticus; ‘‘Pseudos-

tichopus’’ ¼ Pseudostichopus mollis; ‘‘eelpout’’ ¼ Licodichthys sp.

4.00

6.00

8.00

10.00

12.00

14.00

16.00

18.00

-34.00

δ13C

δ15N

Surface Deposit FeedersSubsurface Deposit FeedersSuspension FeedersInvert Predators/ScavengersFish

Phytodetritus

Surface Sediments

Ice Algae

Subsurface Sediment

Net Plankton

Sediment trap material

-12.00-14.00-32.00 -30.00 -28.00 -26.00 -24.00 -22.00 -20.00 -18.00 -16.00

Fig. 4. Stable isotope ratios (d13C versus d15N) of each individual organism analyzed, with ‘‘trophic-shift’’ boxes (3–5% for d15N and 0–1% for d13C) indicating expected

range of values for organisms feeding exclusively on particular sources of organic material.

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low d13C values in phytoplankton and phytodetritus (Fry and Sherr,1984; Wada et al., 1987; Fischer, 1991; Rau et al., 1991b). Both stableisotope data and qualitative microscopic observations of planktonsamples suggest springtime abundance of the diatom Corethron

criophilum in the 1999/2000 bloom season, followed by latesummer/early winter increases in juvenile krill densities (similarto Wada et al., 1987; Fischer, 1991; Frazer, 1996). We observed asimilar abundance of C. criophilum in the following spring planktonsamples (Oct 2000), although the magnitude of the subsequentsummer bloom in early 2001 was much greater than in the previousyear (Ducklow et al., 2006; Smith et al., 2008). Further, d13C valuesof plankton samples from the two summer seasons were markedlydifferent (10%), with the most dramatic difference at Station A(Table 1; Fig. 2). This increase in d13C coincided with a change inthe assemblage of diatoms from the C. criophilum-dominatedcommunity at all stations in Oct 2000. In Mar 2001, we observeda gradient across the shelf, with a community dominated byCoscinodiscus sp. at Station A, to a Rhizosolenia-dominated commu-nity at Station C. d13C enrichments on the order of 10% havebeen reported elsewhere in Antarctic waters, accompanying bothchanges in the phytoplankton assemblage and large increases inprimary production (Fischer, 1991; Dunbar, 1992; Dehairs et al.,1997).

High d13C in Mar 2001 plankton may have been related tohigh productivity rates during the 2000–2001 summer bloom

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Peniagone vignoni

Nov-99Mar-00Jun-00Mar-01surf sed

Protelpidia murrayi

4

5

6

7

8

9

10

11Nov-99Mar-00Jun-00Mar-01surf sed

Promachocrinus kerguelensis

-28

δ13C δ13C

δ15N

δ15N

Nov-99Jun-00Oct-00Mar-01plankton

L. marionensis and Aurospio sp. n.

4

5

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7

8

9

10

11

4

5

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7

8

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10

11δ15

Nδ15

N

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7

8

9

10

11Nov-99Mar-00Jun-00Oct-00Mar-01surf sed

Limopsis marionensis

Aurospio sp. n.

-21-27 -26 -25 -24 -23 -22 -28 -21-27 -26 -25 -24 -23 -22

-28

δ13C δ13C-21-27 -26 -25 -24 -23 -22 -28 -21-27 -26 -25 -24 -23 -22

Fig. 5. Stable isotope ratios (d13C versus d15N) of surface sediments (0–0.5 cm) and body tissue from the surface-deposit-feeding holothurians (A) Peniagone vignoni and (B)

Protelpidia murrayi; (C) net plankton (Jun 2000—primarily zooplankton) and body tissue from the crinoid Promachocrinus kerguelensis; and (D) surface sediments and body

tissue from macrofaunal polychaetes Aurospio sp. n. (gray symbols) and the bivalve Limopsis marionensis (black symbols). Error bars indicate 71 standard error.

Table 3

Seasonal differences in d13C and d15N for Peniagone vignoni (SDF), Protelpidia

murrayi (SDF), and Promachocrinus kerguelensis (SF), based on multivariate ANOVA

post hoc comparisons (least significant difference)

Significant differences for each isotope are marked with C or N, as well as asterisks

representing the significance level (e.g., p ¼ 0.05 (C*), 0.01 (C**), and o0.001

(C***)). d13C comparisons are recorded above the diagonal, and d15N comparisons

are recorded below the diagonal. x ¼ not significant; nd ¼ no data.

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formation, because differences in carbon demand between fast-and slow-growing phytoplankton assemblages can affect carbonfractionation (i.e., high-productivity waters may becomeCO2-limited, resulting in increased d13C) (e.g., Fry and Wainright,1991; Nakatsuka et al., 1992; Canuel et al., 1995). Ducklow et al.(2006) report strong interannual variability in primary productiv-ity near Palmer Station, with total summer bloom (15 Oct–15 Apr)production in 2000–2001 nearly 5 times higher than during theprevious year’s bloom period. While high d13C values are alsocommon in ice algae due to biologically driven CO2(aq) depletionwithin sea-ice (Wada et al., 1987; Hobson et al., 1995; Gibsonet al., 1999), we do not believe ice algae made a significantcontribution to the high d13C signatures found in our net planktonin late summer 2001. Ice algae, including Phaeocystis spp. anddiatoms, tend to aggregate and sink quickly (4200 m d�1), leavingthe upper water column within days to weeks following thebreak-up of winter sea-ice (Riebesell, 1991; DiTullio et al., 2000).Ice had been absent at all our stations for 2–3 months prior to ourMar 2001 sampling (Fetterer and Knowles, 2004), and ice algaewere thus not likely to be present among sinking particulates.Based on the similarity in d13C values between sediment-trapmaterial and summer net plankton, the bulk of the materialreaching the traps appears to have been deposited during summermonths. Trap material collected during summer (Oct–Mar)2000/2001 appeared, under microscopic examination, to consistlargely of the diatom C. criophilum, and had a similar d13Csignature as net plankton from Oct 2000 (��28%), which alsocontained abundant C. criophilum. Sinking fluxes of this diatom inice-edge habitats typically produce comparable d13C values(Bathmann et al., 1991), whereas sedimenting ice algae and krillfecal pellet strings released upon the initial break-up of wintersea-ice measure �20% to �25% (Wada et al., 1987; Fischer, 1991;Frazer, 1996). d13C of sediment-trap material did not resemble icealgae (�19%) in any time period (Table 1), and thus ice algae didnot appear to contribute significantly to sinking POM at our trapdepths (4400 m below surface).

Interestingly, the Oct 2000–Mar 2001 traps contained differentdiatoms (C. criophilum) than those found in the dense phyto-plankton bloom underway in the overlying waters during Mar 01(Coscinodiscus and Rhizoloenia spp.). Further, spring and summer(Nov and Mar) plankton samples in 1999/2000 had similar d13Cvalues, whereas values differed substantially between Oct 2000and Mar 2001, particularly at Stations A and B (Table 1; Fig. 2).Sinking rates for single Antarctic diatom cells are on the order of1–10 m d�1, with larger aggregates typically formed by thesecolonial taxa reaching 20–100 m d�1 (e.g., Priddle, 1990). In2000/2001, the initial spring bloom of C. criophilum may thushave sunk quickly from the surface waters, giving way to asecondary bloom of a different assemblage later in the summer.Consequently, the flux of bloom-derived particles to the benthosmay have continued later into the fall and winter in 2001 than inthe previous year.

The presence of a thick phytodetrital carpet observed only inMar 2001 (Smith et al., 2008) provides further evidence oflarge interannual variability in particle flux on the WAP shelf(Smith et al., 2006; Ducklow et al., 2006). d15N values ofphytodetritus were �2% higher than sediment-trap materialdeposited during the same period (Table 1), suggesting degrada-tion of phytodetrital material at the seafloor and/or dilution withmore refractory sedimentary organic carbon. Dilution seems morelikely, because the high concentrations of Chl-a in phytodetritus(Mincks et al., 2005) indicated the presence of substantialfresh algal material. Despite the temporally patchy nature ofphytoplankton blooms and phytodetritus accumulation duringour study period, surface sediments exhibited minimal variabilityin stable isotope signature, suggesting a buffering effect of

sediments against water column variability (cf., Lovvorn et al.,2005; Mincks et al., 2005).

4.2. Trophic status of benthic megafauna

The benthic community at FOODBANCS sites is typical of muchof the deep, soft-sediment Antarctic shelf, with polychaetes,molluscs, and crustaceans dominating in abundance, and echino-derms dominating the biomass (Lowry, 1975; Muhlenhardt-Siegel,1988; Arnaud et al., 1998; Starmans et al., 1999; Gutt, 2000). Thebroad range in d13C values detected among WAP shelf benthos,combined with a narrow range in d15N (Fig. 3), suggests these taxaoccupy a limited number of trophic levels, and utilize a variety ofdetrital food resources. Wide ranges in d13C values amongdetritivorous benthos were also reported for the Weddell Sea(Nyssen et al., 2002) and Arctic shelves (Hobson and Welch, 1992;Hobson et al., 1995, 2002; Lovvorn et al., 2005).

SDFs had the narrowest range in isotope values in any of thetrophic groups sampled. The elpidiid holothurians Peniagone

vignoni and Protelpidia murrayi, as well as the spionid polychaeteAurospio sp. n., were sufficiently enriched in d15N, suggesting onetrophic level above surface sediments (cf., Michener and Schell,1994) (Fig. 5A, B, D). The synallactid holothurian Pseudostichopus

mollis fell in the same range in d13C, but was 2% more enriched ind15N. It may be less selective for the freshest particles at thesediment surface, or may obtain some material from deepersediment layers. Echiurians were �2% enriched in both 13C and15N relative to other SDFs, and may either be feeding on morerefractory material, or selecting for a particular fraction ofsediment organic matter such as gardened bacteria (cf., Smithet al., 1986; Jumars et al., 1990; Lovvorn et al., 2005). 14C and234Thxs in deposit-feeder gut contents on the WAP shelf indicatehighly efficient particle selectivity in P. vignoni and echiurians,with the greatest selectivity relative to other deposit-feedersoccurring in winter (i.e., Jun 2000) (McClintic et al., 2008;Purinton et al., 2008).

SSDFs spanned the maximum range in d13C (Figs. 3 and 4),with heavy 13C depletion in the irregular urchins (Amphipneustes

lorioli and A. rostratus), and enrichment in head-down deposit-feeding holothurians (Molpadia musculus and Ypsilocucumis turri-

cata). However, our use of gonad tissue probably underestimatedthe d13C value in irregular urchins. Irregular urchins on the WAPshelf undergo continuous reproductive cycles (Galley, 2003;Galley et al., 2005), and consequently had high lipid contentyear-round as indicated by high C:N ratios at the time of oursampling (Table 2). Both lipid content and C:N ratios typicallyshow negative correlations with d13C (DeNiro and Epstein, 1978;McConnaughey and McRoy, 1979; Wada et al., 1987; Rau et al.,1991a), as seen in our data for C:N ratios (R2

¼ 0.667, p ¼ 0.004).Body wall d13C values for irregular urchins reported by Purintonet al. (2008) ranged from �24% to�10%, placing them nearer therange of values we measured for the other SSDFs (��22% to�18%). All the SSDFs were confined to a narrow range in d15Nvalues approximately one trophic level (3–5%) above subsurfacesediments. However, differences in d13C clearly suggest utilizationof a range of organic materials from the sediments (cf., Lovvornet al., 2005).

SDF and SSDF taxa were roughly 2–10% heavier in d13C thanmean plankton values and up to 7% heavier than surfacesediments (Fig. 3), suggesting substantial reworking of sedimentorganic material at the seafloor prior to uptake by benthicmegafauna. d13C enrichments in POM at the sediment–waterboundary ranging from 1% to 4% have been reported on theAntarctic shelf, and are attributed to varying intensity and/ormode of benthic remineralization (Fischer, 1991). Benthic, detri-tus-based food webs typically exhibit greater (4–5%) enrichment

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in d13C relative to POM than pelagic consumers, presumably dueto assimilation of microbial and/or meiofaunal biomass or by-products, and the strong carbon fractionation effects of bacterialmetabolism (McConnaughey and McRoy, 1979; Hobson et al.,1995; Nyssen et al., 2002; Lovvorn et al., 2005). Indeed, data fromthe WAP shelf do indicate potentially extensive reprocessing ofphytodetritus by foraminifera (Suhr et al., 2003).

Low-mobility predators and scavengers (P/S I) fell within a�2% range in d13C and d15N, and were generally enriched in d13Crelative to the more mobile P/S group (P/S II; Fig. 3). This d13Cenrichment is common in omnivores and detritivores, and mayreflect assimilation of recycled detrital carbon along with carbonfrom fresh tissue (Hobson et al., 2002). These taxa may also feedon small invertebrates. However, most of the taxa in P/S I wereo2% higher in d15N than macrofaunal polychaetes. Their dietsmay include a mixture of detritus and macrofaunal prey items.Larger, more mobile predators and scavengers (P/S II), such as fishand octopus, spanned a much larger range in d15N, covering atleast two trophic levels (Fig. 3). This range constitutes a fairlylinear relationship reminiscent of a classic pelagic predatory foodchain (e.g., Brooks and Dodson, 1965; Ryther, 1969). The lowerd13C values combined with the wider range in d15N in P/S IIsuggest at least partial dependence on pelagic food sources suchas zooplankton, which tend to have lower d13C values (Wada et al.,1987; Frazer, 1996).

Separation between pelagic and benthic feeding groups hasbeen observed elsewhere at high latitudes (McConnaughey andMcRoy, 1979; Hobson et al., 1995, 2002), and may be responsiblefor the 4% difference in d13C between the two anemones,Hormathia lacunifera and Isosicyonis alba (Fig. 3). I. alba livesobligatorily on the shell of the gastropod Harpovoluta charcoti,which also differed from I. alba by about 4% in d13C. I. alba’s stableisotope signature places it roughly in the range that would bepredicted for organisms feeding on juvenile krill (net planktonvalues for Jun 2000, Table 1; see also Frazer, 1996). Thus, I. alba

and H. lacunifera appear to be capitalizing on quite different foodsources, with the latter likely deriving food from the detritus-based benthic system. Substantial trophic separation is alsoevident between I. alba and its gastropod host, H. charcoti, whichis said to feed on carrion (Arnaud, 1978).

Ctenocidaris perrieri, the ‘‘pencil urchin’’, is somewhat anom-alous among the benthos examined here, with an extremely highd15N of �16%. Cidarid urchins on the Antarctic shelf are reportedto feed on other invertebrates, including molluscs, sponges, andhydroids (Jacob et al., 2003), although Galley (2003) reportedsediment in C. perrieri guts. Biochemical analysis of C. perrieri

tissues indicates winter periods of starvation (Galley, 2003), andstarvation conditions also can produce elevated d15N values(Fantle et al., 1999). Alternatively, C. perrieri could have acarrion-rich diet. Similar d15N enrichment has been noted inscavenging amphipods from the Weddell Sea, known to feed onfish and crustacean remains (Nyssen et al., 2002).

Given the dominance of deposit-feeders on the WAP shelf, wecollected few suspension-feeders in sufficient abundance forstable isotopic analyses. The crinoid, Promachocrinus kerguelensis,yielded stable isotope values very similar to those of I. alba (Fig. 3).Such values again suggest juvenile krill or other zooplankton aspotential food sources. The sponge C. antarctica yielded curiousstable isotope values, similar to C. perrieri (Fig. 3). Cinachyra

antarctica was enriched in d13C relative to plankton and fell withinthe range of the detritivores, but d15N values were the highestrecorded in our study. Because this sponge is unlikely to be anapex predator on the WAP shelf, high d15N values may be relatedto relatively indiscriminate filtering of particulate material fromthe water column, potentially including a variety of material suchas bacteria and their exudates (Iken et al., 2001; Nyssen et al.,

2002). The bivalve Limopsis marionensis is also most likely asuspension-feeder (Oliver, 1979), but stable isotope values place itin the midst of the deposit-feeders (Fig. 3), suggesting feeding onresuspended sediment. In shallower waters around the PrinceEdward Islands, L. marionensis yielded d15N values �5% lowerthan those shown here, likely due to feeding directly onphytoplankton (Kaehler et al., 2000).

The soft-sediment benthic community on the WAP shelfappears to be composed of two groups of organisms—one groupderiving nutrition primarily from sediments or detritus at theseafloor, and one utilizing epibenthic or pelagic food resourcessuch as zooplankton (Fig. 6). Most organisms fell between 7% and11% in d15N, which is roughly within the range of values reportedfor Weddell Sea benthos (Nyssen et al., 2002), and suggestsapproximately two trophic levels between POM and benthos.Hobson et al. (1992, 1995, 2002) reported a similarly narrow rangein d15N for Arctic benthos, as well as a lack of dependence on icealgal food sources as seen here. This finding is somewhatsurprising given recent evidence of a preference for ice algae insome near-shore Arctic deposit-feeders (McMahon et al., 2006).Stable isotope values for benthic communities in shallowerAntarctic shelf regions (intertidal to 170 m) showed less enrich-ment in d15N in several of the same taxa sampled here(e.g., bivalves, scale worms), apparently due to increaseddependence on macroalgal food sources and/or direct grazingon pelagic phytoplankton (Kaehler et al., 2000; Dunton, 2001).However, holothurians and some larger predators such asoctopus showed values similar to our WAP shelf sites (Kaehleret al., 2000).

4.3. Temporal patterns in detritivore feeding

Benthic fauna on the WAP shelf are thought to experiencereduced seasonality in food availability relative to pelagicorganisms (Gutt, 2000; Mincks et al., 2005; Smith et al., 2006),as evidenced by the year-round appearance of relatively freshdetrital carbon in deposit-feeder guts (Galley, 2003; Purintonet al., 2008). Dampened seasonal and interannual changes instable isotope signatures of sinking particulates and sedimentslend additional support to these observations. Thus, even if carbonand nitrogen turn over rapidly in body tissues (cf., Lorrain et al.,2002; Rossi et al., 2004; McMahon et al., 2006), we would expectbenthic detritivores to show relatively little temporal variation instable isotope signature, despite the pulsed nature of organicinputs to the sediments.

The surface-deposit-feeding holothurians Peniagone vignoni

and Protelpidia murrayi were usually found with full guts duringall of our cruises (Galley, 2003), and appeared to be feeding year-round. P. vignoni in our study area is a highly selective feeder, ableto ingest young, apparently fresh material in all seasons, whereasP. murrayi utilizes selective degradation/assimilation to enhancenutritional value from less selectively ingested sediments(Purinton et al., 2008). Both taxa had similar average isotopevalues (Fig. 3). However, temporal patterns in d13C differedbetween the two species, with P. murrayi showing greaterseasonal variability in d13C (Fig. 5A and B; Table 3). This variabilitymay be due to seasonal changes in the proportion ofsurface sediments composed of relatively fresh detritus (see alsoWigham et al., 2008). In other words, P. vignoni is able toselect and ingest the highest food-quality particles, evenwhen they are less abundant, whereas P. murrayi ingests sedi-ment less discriminately, digesting particular sedimentarycomponents, including bacteria and their exudates. Lovvornet al. (2005) proposed selective use of bacteria as an explanationfor heavy 13C-enrichments in some detritivores on the Arctic shelf.Interestingly, maximum 13C values in P. murrayi occurred in Nov

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1999 and Mar 2001, concurrently with peaks in microbial biomass(Mincks et al., 2005).

In contrast to the holothurians, the macrofaunal spionidpolychaete Aurospio sp. n. did not exhibit temporal variability inisotopic signature over the three seasons sampled (Fig. 5D).Smaller organisms tend to equilibrate faster to seasonal changesin diet (e.g., Schmidt et al., 2003), so this species should berelatively sensitive to seasonal changes in the isotopic value offood. However, mean isotope values for spionids were very similarto those for both holothurians described above, suggesting asimilar source of food particles for all these SDFs. Smaller(macrofaunal) deposit-feeders like Aurospio sp. n. may beconstrained by gut size to utilize greater particle-selectivity thanlarger organisms such as the holothurians, in order to maximizenutritional intake (Jumars et al., 1990). In any case, food-richparticles appear to be available to particle-selective SDFs year-round on the WAP shelf in our study area.

The bivalve Limopsis marionensis also exhibited no seasonalvariability in stable isotope signatures (Fig. 5D). However, isotopevalues in this species were 2–3% enriched in 13C and 15N relativeto the other taxa described above, suggesting a more refractoryor recycled carbon source. The feeding mode in L. marionensis

is not definitively known, although many of the presumably

suspension-feeding deep-sea bivalves are members of this genus(Allen, 1979; Oliver, 1979). This species more closely resemblesdeposit-feeding echiurians in stable isotope values, suggesting asediment-derived food source such as resuspended sedimentparticles. Minimal temporal variability in L. marionensis maythus reflect the lack of seasonal change in stable isotope valuesof surface sediments (Fig. 2), consistent with a sediment foodbank.

While some seasonal variations in d15N were found in thesuspension-feeding crinoid Promachocrinus kerguelensis, thesevariations were relatively small (Fig. 5C) and mainly occurredbetween winter and spring/summer (Table 3). Crinoids alwaysfell within one trophic level above net plankton (Fig. 5C),and variations in crinoid tissues could thus reflect seasonaland/or ontogenetic shifts in stable isotopic signatures of krilland other zooplankton prey items (cf., Frazer, 1996; Schmidt et al.,2003).

4.4. Summary and implications for benthic–pelagic coupling

on the WAP shelf

Our results suggest that the bulk of sedimenting organicmaterial on the WAP shelf is derived from the summer

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DIATOMSICE ALGAE

SEA ICE

ZOOPLANKTON

PARTICLE-SELECTIVE SDFs

LESS SELECTIVE SSDFs

SEDIMENT INFAUNA

MOBILE PREDATORS

SUSPENSION FEEDERS

RESUSPENDED SEDIMENT

INVERTEBRATE PREDS/SCAVS

Fig. 6. Simplified food web on the deep (�500 m), soft-sediment West Antarctic Peninsula continental shelf. Arrows point from prey to consumer. At FOODBANCS stations,

suspension-feeders feeding on resuspended sediment include Limopsis marionensis and sponges, and those feeding on plankton include Isosycionis alba and Promachocrinus

kerguelensis. ‘‘Mobile predators’’ include epibenthic fish and octopus. ‘‘Invertebrate predators/scavengers’’ include Hormathia lacunifera, gastropod mollusks, Ctenocidaris

perrieri, and Laetmonice producta. Highly particle-selective surface deposit-feeders include the holothurians Peniagone vignoni and Protelpidia murrayi, as well as the infaunal

spionid polychaetes Aurospio sp. n.; less selective deposit-feeders include irregular urchins, and the holothurians Molpadia musculus, Pseudostichopus mollis, and

Ypsilocucumis turricata.

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phytoplankton bloom, and arrives with relatively minimaldegradation at the seafloor. Substantial temporal and spatialvariability occurred in the stable isotope signature of net-collectedplankton, but was not observed in surface sediments (Fig. 2).Benthic megafauna exhibited a broad range in d13C values, butmost taxa fell within a narrow range in d15N, resembling a‘‘trophic continuum’’ (France et al., 1998) rather than a classiclinear food chain (Fig. 3). While the spionid polychaetes andthe bivalve L. marionensis exhibited constant stable isotopesignatures year-round, surface-deposit-feeding holothurians(especially P. murrayi; Fig. 5B) and the suspension-feeding crinoidP. kerguelensis (Fig. 5C) revealed temporally varying stable isotopesignatures, reflecting temporal patterns in sedimenting POM.These taxa were substantially (3–6%) heavier in d15N than trapmaterial and surface sediments, and appear to be derivingnutrition from bloom detritus. However, given the lack ofseasonality in isotopic values of surface sediments, seasonalityin SDFs suggests substantial selectivity for components of thefreshly deposited organic material.

The low d15N values of sediment-trap samples, particularly inthe period from Nov 1999 to Mar 2000 (Fig. 2), suggest thatrelatively undegraded algal material was captured in the traps.Sedimentation of fresh algal material to within 150 m of theseabed points to rapid sinking of bloom material during thisperiod, such that minimal degradation occurred in the watercolumn. This rapid sinking should have resulted in the delivery ofa highly labile food source for the benthos. Further, d15Nenrichment in polar shelf benthos reported here and by others(e.g., Hobson et al., 1995, 2002; Dunton, 2001; Nyssen et al., 2002)is typically low compared to deep-sea areas of phytodetritusdeposition such as the Porcupine Abyssal Plain (Iken et al., 2001).This pattern strongly suggests that fresh algal material rapidlysinks to the seafloor during summer with minimal degradationin the water column, and enters the benthic food web (Fig. 6)(see also Mincks et al., 2005; Smith et al., 2008).

While d13C signatures of plankton samples varied by as muchas 14% over the course of this study, and sediment-trap materialby more 3.4%, d13C values in surface sediments only varied byabout 2% (Fig. 2). The close connection between d13C values insediments and detritivores (Fig. 4) suggests that bloom-derivedmaterial is incorporated into the sediment and remains availableto consumers throughout much of the year. Thus, stable isotopedata lend additional credence to the hypothesis that a food bankof labile material persists year-round in Antarctic shelf sediments(cf., Mincks et al., 2005; Smith et al., 2006, 2008). In addition, ourdata suggest WAP shelf sediments and resident detritivores mayintegrate short-term (seasonal to interannual) variability in fluxevents, exhibiting substantial ‘‘inertia,’’ and potentially respond-ing to ecosystem changes over longer time scales (e.g., years todecades) (Smith et al., 2006).

Acknowledgments

We greatly appreciate the help of various cruise participants insample collection, including D. DeMaster, T. Ferrero, N. Mitchell, E.Galley, A. Glover, M. McClintic, A. Demopoulos, A. Baco-Taylor, M.Parry, E. Ramirez, and M. Baker. We also acknowledge theinvaluable support of Raytheon Polar Services personnel, andthe crews of the R.V. L.M. Gould and R.V. N.B. Palmer. T. Rust andJ. Tanimoto were instrumental in the timely analysis of stableisotope samples. This project was supported by grants fromthe National Science Foundation, Office of Polar Programs andBiological Oceanography Program to C.R.S. and David J. DeMaster.This is contribution #7532 from SOEST, University of Hawai’iat Manoa.

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