Continental Shelf Research 35 (2012) 53–63

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Continental Shelf Research

0278-43

doi:10.1

n Corr

E-m

journal homepage: www.elsevier.com/locate/csr

Research papers

Benthic macrofauna assemblages and biochemical properties of sediments intwo Antarctic regions differently affected by climate change

E. Sane a,n, E. Isla a, D. Gerdes b, A. Montiel c, J.-M. Gili a

a Instituto de Ciencias del Mar (ICM-CSIC), Paseo Marıtimo de la Barceloneta 37-49, 08003 Barcelona, Spainb Alfred Wegener Institute for Polar and Marine Research, Columbustrasse, D-27568 Bremerhaven, Germanyc Universidad de Magallanes, Instituto de la Patagonia, Av. Bulnes 01855, 621-0427 Punta Arenas, Chile

a r t i c l e i n f o

Article history:

Received 1 June 2011

Received in revised form

5 September 2011

Accepted 16 December 2011Available online 28 December 2011

Keywords:

Biochemistry

Sediments

Macrofauna

Antarctica

43/$ - see front matter & 2012 Elsevier Ltd. A

016/j.csr.2011.12.008

esponding author.

ail address: sane@icm.csic.es (E. Sane).

a b s t r a c t

Lipid, protein and carbohydrate concentrations have been determined in sediment cores from the

continental shelf in the South Eastern Weddell Sea (SEWS), where no ice shelves have been present at

least for thousands of years, and the continental shelf off the Eastern Antarctic Peninsula (EAP), in the

area where two ice shelf collapses occurred in 1995 and 2002. On one hand, SEWS presents an

important flux of fresh organic matter to the seabed during summer, whereas on the other hand, the

presence of ice shelves in EAP hampered photosynthesis restricting the input of organic matter to

advected refractory material. In the present study, biochemical variables and benthic macrofauna

abundance, biomass and diversity confirmed differences between the two regions. Lipid concentrations

were higher in SEWS than in EAP, whereas carbohydrate concentrations were higher in the latter

region. These differences were attributed to the higher concentration of labile and refractory material,

respectively. Biomass, abundance and diversity of the macrofauna were higher in SEWS than in EAP,

where benthic communities started receiving a fresh organic matter input only after the recent ice shelf

collapses. As regards macrofauna composition, both regions presented macrobenthic communities

associated to early stages of recolonization.

& 2012 Elsevier Ltd. All rights reserved.

1. Introduction

The quantity and quality of the organic matter (OM) reachingthe seabed are important for benthic communities (Thompsonand Nichols, 1988; Graf, 1989; Dugan et al., 2003) since theyrepresent the principal factors regulating benthic biomass(Grebmeier et al., 1988). Benthic community abundance anddiversity are positively correlated with protein (PRT), carbohy-drate (CHO) and lipid (LPD) concentrations in the sediment(Fabiano and Danovaro, 1999; Albertelli et al., 1999; Dell’Annoet al., 2000; Medernach et al., 2001; Neira et al., 2001; Gremareet al., 2002). PRT and diatom storage CHO are easily degraded bybacteria in the water column and in the superficial sediment(Handa and Yanagi, 1969; Berland et al., 1970; Liebezeit, 1984;Ittekkot and Arain, 1986) while LPD and water-insoluble CHOhave a higher chemical stability (Handa and Tominaga, 1969;Toth and Lerman, 1977).

In Polar Regions, ice coverage at the sea surface hampers primaryproduction (Arrigo et al., 2002; Arrigo and van Dijken, 2003), limitingthe OM flux to the seafloor. From 1946 to 2006, atmospheric

ll rights reserved.

temperatures have risen at þ0.41 1C per decade on the eastern sideof the Antarctic Peninsula (SCAR’s Antarctic Climate Change and theEnvironment (ACCE) Review Report). As a consequence of the recenttemperature increase in the atmosphere (Vaughan et al., 2001),4200 km2 of the Larsen A ice shelf disintegrated in January 1995(Rott et al., 1996) and 3200 km2 of the Larsen B ice shelf collapsedwithin 33 day in March 2002.

Based on the idea that climate change forces the environ-mental characteristics that ultimately modify the ecosystem, weinvestigate how Antarctic continental shelf ecosystems respondto climate change by comparing the sediment biochemical char-acteristics and the macrofauna off the Eastern Antarctic Peninsula(EAP) coast, where Larsen A and B ice shelf collapses recentlyoccurred, and in the South Eastern Weddell Sea (SEWS) con-tinental shelf, which has not been covered by shelf ice at least forthousands of years (Ingolfsson et al., 1998; Anderson et al., 2002).

2. Materials and methods

2.1. Study area

The study area comprises the two extremes of the WeddellSea, one area in the SE and another in the NW (Fig. 1). In the south

Eastern AntarcticPeninsula (EAP) Southeastern Wedell

Sea (SEWS)

60°S

63°S

70°S

77°S

84°S

0°21°W42°W63°W84°W

60°W64°W68°W72°W

66°S

64°S

68°S

62°S

70°S

71°S

72°S

6°W8°W10°W12°W

Ice shelf

Ice shelf

SEWS

Fig. 1. (a) Study area. (b) EAP and SEWS regions with sampling stations.

E. Sane et al. / Continental Shelf Research 35 (2012) 53–6354

eastern Weddell Sea, typical Antarctic seasonal conditionsdevelop open water characteristics, high primary production ratesand intense organic matter pulses to the seabed during the australsummer (Bathmann et al., 1991; Isla et al., 2009). Pulses aremainly constituted by diatoms and fecal pellets, which transportfresh, lipid-rich organic matter to the seabed (Schnack-Schiel andIsla, 2005; Isla et al., 2006). This area is also known to undergoheavy iceberg transit (Gutt and Starmans, 2001), which erodes thesea floor enhancing the local macrobenthic community dynamics(Gutt and Starmans, 2001; Gerdes et al., 2003, 2008). On the otherside, in the northwestern Weddell Sea, after thousands of years ofstability, anthropogenic global warming is causing the collapse ofmassive sections of ice shelves (Domack et al., 2005). Theenvironmental characteristics of this area are rather unknown incomparison to the southeastern extreme; however, it is knownthat in the northwestern Weddell Sea primary production starteddeveloping after the collapse of the ice shelf (Bertolin and Schloss,2009) with the consequent flux of fresh organic matter to the seafloor (Sane et al., 2011a). The Weddell Gyre’s cyclonic circulationconnects the two regions investigated in this study (Fahrbachet al., 1994). The mean flow of the Weddell Gyre decays in thenorthern rim and then reforms in the south, favouring particlestransport from the south eastern Weddell Sea to the tip of theAntarctic Peninsula (Fahrbach et al., 1994; Schrodemr andFahrbach, 1999). In the Weddell Sea, the distribution pattern of

glacial–marine surface sediments with different mineralogicaland granulometric properties has been related to the WeddellGyre current transport, which may carry fine particles from thesoutheast to the northwest (Dieckmann and Kuhn, 1999).We want to compare the two extremes of the Weddell Sea basedon the notion that the ice characteristics represent the mostimportant differences in their respective geophysical histories.

2.2. Sample collection

Samples were collected from the continental shelf duringexpeditions ANT XXI/2 and ANT XXIII/8 in austral summers 2003–2004 and 2006–2007, respectively, onboard the R/V Polarstern. Foursediment cores (stations 76, 77, 80 and 82) were collected in SEWSduring ANT XXI/2, and four sediment cores (stations 700, 703, 714and 725) were collected in EAP during ANT XXIII/8 (Fig. 1 andTable 1). Sediment samples were taken with a multi-corer (Barnettet al., 1984), and macrobenthic samples were collected with amultibox corer (Gerdes, 1990).

2.3. Sediment biochemistry

Sediment cores were subsampled onboard in slices 0.5 cmthick from the top to 7.5 cm depth and stored at �20 1C until theycould be analyzed in the laboratory. Before biochemical analyses,

Table 1Sampling expedition, year and season, region, station, coordinates and depth.

Expedition Sampling year and season Region Station Core length (cm) Latitude Longitude Depth

ANT XXI/2 2003–2004 Summer SEWS 76 8 70122.970 9122.320 489

ANT XXI/2 2003–2004 Summer SEWS 77 8 70126.080 09115.320 311

ANT XXI/2 2003–2004 Summer SEWS 80 8 70128.270 09111.710 343

ANT XX/2 2003–2004 Summer SEWS 82 8 70131.510 09106.280 421

ANT XXIII/8 2006–2007 Summer EAP 700 11 65155,110 60120.140 446

ANT XXIII/8 2006–2007 Summer EAP 703 11 65133,000 61137.150 297

ANT XXIII/8 2006–2007 Summer EAP 714 11 6516,400 60145.010 322

ANT XXIII/8 2006–2007 Summer EAP 725 7.5 64155,730 60137.230 239

mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

Dep

th (c

m)

CHOPRTLIP

0 2 4 6 8 0 2 4 6 80 2 4 6 8 0 2 4 6 8mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

EAP

mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

Dep

th (c

m)

mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

0 2 4 6 80 2 4 6 8 0 2 4 6 8 0 2 4 6 8mg g-1 DW

7.57

6.56

5.55

4.54

3.53

2.52

1.51

0.50

SEWS

stn. 700 stn. 703 stn. 714 stn. 725

stn. 76 stn. 77 stn. 80 stn. 82

Fig. 2. CHO, PRT and LIP concentration (mg g�1 DW) vertical profiles in SEWS and EAP stations.

E. Sane et al. / Continental Shelf Research 35 (2012) 53–63 55

sediment was freeze dried (P¼0.1 mbar and T¼�80 1C) for 24 hand macrobenthic organisms were picked out under binocular.

LPD, CHO and PRT analyses were carried out in triplicate andstandard deviations of the three replicates were represented witherror bars (Fig. 2). For each sample, a blank analysis (sediment treatedduring 4 h at 450 1C) was also performed. LPD were quantifiedfollowing the Barnes and Blastock procedure (Barnes andBlackstock, 1973) using cholesterol as a standard, CHO followingthe Dubois procedure (Dubois et al., 1956) using glucose as a standardand PRT following the Lowry procedure (Lowry et al., 1951) asmodified by Rice (1982) using albumin as a standard. Absorbancewas measured with a Shimadzu spectrophotometer at 520 nm forLPD, 485 nm for CHO and 750 nm for PRT. Concentrations of LPD,CHO or PRT should be considered as cholesterol, glucose and albuminequivalents. LPD, CHO and PRT concentrations are expressed asmilligrams per gram sediment dry weight (mg g�1 DW).

2.4. Macrobenthos

All samples were sieved on a 500 mm mesh and preserved in a4% formaldehyde–seawater solution buffered with hexamethy-lentetramine. To characterize the benthic community, the number

of organisms (N m�2) and the biomass (mg WW m�2) werequantified. The wet weight was determined using a Sartoriusbalance (model R 180 D). In the benthic community, classesDemospongiae, Hydrozoa, Anthozoa, Gasteropoda, Bivalvia,Scaphopoda, Polychaeta, Echiurida, Pycnogonida, Ostracoda,Echinoidea, Holothuroidea, Asteroidea, Ophiuroidea and Tunicatawere identified.

The Simpson diversity index (Margalef, 1958; Menhinick,1964) was calculated for abundance and biomass of SEWS andEAP benthic communities.

2.5. Sediment granulometry

Peroxide (7%) pre-treated samples of wet sediment weresuspended in milli-Q water with the Hydro Mu (Malverns) andgrain size analyses were carried out using a Mastersizer 2000(Malverns) laser micro-granulometer.

2.6. Multivariate statistical analyses

Biochemistry and macrofauna data were statistically treated usingPRIMER 6 and PERMANOVAþsoftware (Clarke, 1993; Anderson,

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

CH

O (m

g g-1

DW

)

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

PRT

(mg

g-1 D

W)

SEWSEAP

SEWSEAP

Depth (cm)

0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.5

Depth (cm)

0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.5

Depth (cm)

0 0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7 7.50

0.5

1

1.5

2

2.5

3

3.5

4

4.5

LIP

(mg

g-1 D

W)

SEWSEAP

Fig. 3. Linear regressions between CHO, PRT and LIP concentration (mg g�1 DW) and depth in SEWS and EAP stations.

Table 2Main characteristics of regression lines of CHO, PRT and LPD concentrations

(mg g�1 DW) and depth in SEWS and EAP.

n R2 P Slope Intercept

CHO SEWS 17 84.875 o0.0001 �0.127 1.587

CHO EAP 17 51.223 o0.01 �0.051 1.938

PRT SEWS 17 80.491 o0.0001 �0.060 0.744

PRT EAP 17 85.582 o0.0001 �0.088 0.748

LIP SEWS 17 91.410 o0.0001 �0.336 3.433

LIP EAP 17 70.371 o0.0001 �0.060 0.559

Table 3Abundance and biomass in the eight stations, 76, 77, 80, 82, 700, 703, 714, 725,

and average values in the two regions NAP and EAP.

Abundance (N m�2) Biomass (mg WW m�2)

Station 76 1936 45,668

Station 77 1128 27,891

Station 80 2001 211,538

Station 82 1746 53,901

Region SEWS 1703 84,749

Station 700 1823 7813

Station 703 695 13,104

Station 714 1054 21,590

Station 725 653 28,970

Region EAP 1056 17,869

E. Sane et al. / Continental Shelf Research 35 (2012) 53–6356

2001; Clarke and Gorley, 2006). Biochemistry data were Square roottransformed and macrofauna data Fourth root transformed to down-weight contributions from quantitatively dominant macromoleculesor macrofauna classes, respectively. Multi-dimensional scaling (MDS)plots were created to represent pairwise data similarities as distancesbetween points in a low dimensional space. For biochemistry data,Euclidean distances between couples of samples were calculated toobtain a triangular distance matrix, whereas, as regards macrofaunaabundance and biomass data, MDS plots were created based on BrayCurtis similarity resemblance matrices. Similarity contours from thecluster analysis were overlaid on the MDS plots. Differences betweena priori-defined groups (regions SEWS and EAP) were tested runningpermutation tests with PERMANOVA (PERmutational MultivariateANalysis Of VAriance) software. PERMANOVA designs with ‘‘region’’as factor were created for biochemistry and macrofauna data. Thehighest possible number of permutations was performed (999 forbiochemistry data and 35 for macrofauna data). For macrofauna data,due to the low number of possible permutations (35), the MonteCarlo asymptotic P-value, P(MC), was used instead of the permutationP-value. For biochemistry data, due to the high number of permuta-tions (999), the Monte Carlo P-value and the permutation P-valuewere the same. The similarity percentages (SIMPER) analysis wascarried out to describe the contribution of macromolecules andmacrofauna classes to similarities within and dissimilarities betweenregions. Finally, the BEST (Bio-EnvþStepwise) routine was run to findthe subset of environmental variables that best ‘‘explains’’ thebiological pattern. Square root transformed biochemical data werestandardised before running the BEST routine.

3. Results

3.1. Sediment biochemistry

At all depths in the sediment column, CHO was the mostabundant compound in all EAP cores and LPD was the mostabundant compound in three of the four SEWS cores (Fig. 2).Based on regional averages, in the superficial sediment (0–0.5 cmdepth) LPD concentrations were higher in SEWS than in EAP(average concentration 4.1570.22 mg g�1 DW in SEWS and0.7570.08 mg g�1 DW in EAP), whereas CHO concentrationswere higher in EAP than in SEWS (average concentration2.2670.12 mg g�1 DW in EAP and 1.7170.10 mg g�1 DW inSEWS). PRT concentrations were similar in both regions (averageconcentration 0.8070.05 mg g�1 DW in SEWS and 0.9870.06 mg g�1 DW in EAP) (Fig. 3). Regression line slopes of LPD,CHO and PRT concentrations as a function of depth were

significantly correlated in both regions (Table 2). CHO and LPDconcentrations had a higher negative slope in SEWS than in EAPwhile PRT concentrations presented a higher slope in EAP than inSEWS (Table 2).

3.2. Macrobenthos

The mean total number of organisms in SEWS (1703 N m�2)almost doubled the mean total number of organisms in EAP(1056 N m�2), whereas the mean total biomass value in SEWS(84,749 mg WW m�2) was approximately four times higher thanthe mean total biomass value at EAP (17,869 mg WW m�2)(Table 3). The class Polychaeta was the most abundant in bothregions (Fig. 4a). Demospongiae, Polychaeta, Echiurida,Holothuria and Ophiurida showed high biomasses in EAP whileDemospongiae, Polychaeta, Anthozoa and Asteroidea showedhigh biomasses in SEWS (Fig. 4b).

For both abundance and biomass data, the Simpson index washigher in EAP than in SEWS (abundance data: Simpson index 0.51

0 20 40 60 80 100%

EAP

SEWS

stn. 700stn. 703stn. 714stn. 725

stn. 76stn. 77stn. 80stn. 82

0 20 40 60 80 100%

BivalviaDemospongiaeHydrozoaAnthozoaGasteropodaScaphopodaEchiuridaOstracodaPolychaetaEchinoideaHolothuroideaAsteroideaOphiuroideaTunicataPygnogonida

EAP

SEWS

0 20 40 60 80 100%

EAP

SEWS

stn. 700stn. 703stn. 714stn. 725

stn. 76stn. 77stn. 80stn. 82

0 20 40 60 80 100%

BivalviaDemospongiaeHydrozoaAnthozoaGasteropodaScaphopodaEchiuridaOstracodaPolychaetaEchinoideaHolothuroideaAsteroideaOphiuroideaTunicataPygnogonida

EAP

SEWS

Fig. 4. (a) Relative abundance of principal taxonomic groups in SEWS and EAP. (b) Relative biomass of principal taxonomic groups in SEWS and EAP.

E. Sane et al. / Continental Shelf Research 35 (2012) 53–63 57

for SEWS and 0.55 for EAP; biomass data: Simpson index 0.36 forSEWS and 0.43 for EAP).

3.3. Sediment granulometry

The percentage of sediment with a grain size o63 mm (silt andclay) was higher in EAP than in SEWS (from �70 to �95% in EAPand from �30 to �60% in SEWS) (Fig. 5). Except for station 77 inSEWS, the percentage of sediment with a grain size o63 mm wasrather constant with depth in both regions (Fig. 5).

3.4. Multivariate statistical analyses

MDS plots of biochemical data (Fig. 6a), abundance data(Fig. 6b) and biomass data (Fig. 6c) showed differences betweenSEWS and EAP regions. The similarity contours from the clusteranalysis differentiated the two regions (Fig. 6a–c). Permutationtests with PERMANOVA software evidenced significative differ-ences between EAP and SEWS regions, both in terms of sedimentsbiochemistry and macrofaunal assemblages (Table 4). The F valuefor biochemistry data is 124.18 (Table 4a). Using a significancelevel (a) of 5%, the critical value for F is much lower than the teststatistic F value (124.18), and the null hypothesis of no differencein sediments biochemistry between SEWS and EAP regions shouldbe rejected. The P value for the F value of 124.18 is 0.001(Table 4a), so the test statistic is significant at the 5% significancelevel. The F value for macrofauna data is 5.6766 (Table 4b). Usinga significance level (a) of 5%, the critical value for F (5.987) ishigher than the test statistic F value (5.6766), and the nullhypothesis of no difference in macrofauna characteristicsbetween SEWS and EAP regions cannot be rejected. Nevertheless,using a significance level (a) of 10%, the critical value for F (3.776)is lower than the test statistic F (5.6766), and the null hypothesisof no difference in macrofauna characteristics between SEWS andEAP regions is rejected. The P(MC) value for the F value of 5.6766

is 0.034 (Table 4b), so the test statistic is significant at the 10%significance level.

From the SIMPER analysis, LPD contributed more than CHOand PRT to the intra-region similarity in both regions (37.91% inEAP and 77.50% in SEWS) and to the inter-regions dissimilarity(77.75%) (Table 5). As regards macrofauna abundance, in both EAPand SEWS, class Polychaeta contributed most to the intra-regionsimilarity (30.53% in EAP and 25.93% in SEWS), whereasHolothuroidea represented the class, which contributed most todissimilarity between regions (14.07%). Finally, as regards macro-fauna biomass, class Polychaeta contributed most to the intra-region similarity in both regions (30.35% in EAP and 21.95% inSEWS) and Echinodea contributed most to the inter-regionsdissimilarity (13.72%) (Table 6).

The BEST routine was used to estimate how macromoleculesconcentration in sediments could be related to the abundance andthe biomass of the macrofauna in EAP and in SEWS. The Spearmancoefficient (r) was calculated to test the strength of the correla-tion between biochemical and macrofaunal data, and whether apositive or negative correlation exists; the Spearman coefficientcan vary between �1 and 1, with the extreme values correspond-ing to complete opposition (�1) or complete agreement (1). TheBEST test showed that, both in EAP and SEWS, LPD representthe biochemical variable, which best ‘explains’ the structure ofthe macrofauna both in terms of abundance and also, togetherwith PRT, in terms of biomass (Table 7).

4. Discussion

Very little is known about environments beneath ice shelvesand their transformations after ice shelf collapses (Domack et al.,2005). This work aims to characterize the biogenic matter presentin the seabed sediment and to study its relation with the benthicmacrofauna beneath collapsed ice shelves, only after less thantwo decades since the collapse. This research represents an

%

4

3

2

1

0

Dep

th (c

m)

% % %

SEWS: stn. 76 SEWS: stn. 80 SEWS: stn. 82SEWS: stn. 77

%

4

3

2

1

0

Dep

th (c

m)

% %

0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100

0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100%

EAP: stn. 700 EAP: stn. 703 EAP: stn. 714 EAP: stn. 725

<63 µm <63 µm <63 µm<63 µm

mµ36<mµ36< <63 µm <63 µm

>63 µm >63 µm >63 µm >63 µm

>63 µm

>63 µm >63 µm

>63 µm

Fig. 5. Sediment grain size in SEWS and EAP.

E. Sane et al. / Continental Shelf Research 35 (2012) 53–6358

advance in the knowledge of life developing beneath collapsed iceshelves and is important to determine the response of Antarcticecosystems to global climate change and to improve the under-standing of Antarctic ecosystems functioning.

4.1. Sediment biochemistry differences between EAP and SEWS

Samples from the Eastern Antarctic Peninsula (EAP) and theSouth Eastern Weddell Sea (SEWS) were obtained during theaustral summer; therefore, differences in the organic matter (OM)content in the sediment linked to the marked Antarctic season-ality at the sea surface should be minimal. Furthermore, allsamples were collected on the continental shelf between �240and �490 m water depth and showed no statistical difference(p¼0.3142) between regions (326 m787 m water depth for EAPand 391780 m water depth for SEWS). If we assume that thetransport of the OM produced through primary production fromthe euphotic zone to the seabed had a larger vertical than lateralcomponent, OM degradation in the water column should havebeen similar in the eight stations. The main difference betweenthe two regions regarding the OM supply to the seabed is that EAPhas been free of ice shelf influence only since a decade, whereasSEWS region for at least a thousand years (Ingolfsson et al., 1998;Anderson et al., 2002).

Ice coverage hampers primary production (PP) (Arrigo et al.,2002; Arrigo and van Dijken, 2003) and consequently the OM fluxto the seafloor. Even if some authors studying the Ross Ice Shelfsuggested that chemosynthesis may provide a small amount ofenergy for benthic organisms under ice shelves (Horrigan, 1981),PP under ice shelves is considered to be very low (Grebmeier and

Barry, 1991; Thomas et al., 2008), making laterally advected OMthe principal food input for such benthic communities (Grebmeierand Barry, 1991). After Larsen A and B ice shelf collapses, PP inEAP water column started developing (Bertolin and Schloss, 2009)and consequently the phytoplankton detritus flux to the seafloor(Domack et al., 2005; Sane et al., 2011a). This flux represents ahigh percentage of the POM reaching the seafloor (Fischer et al.,1988) and is typically composed by heterotrophic bacteria, fecalpellets and abundant unicellular algae (Arrigo et al., 1995), whichare released during pack ice breakage and melting (Legendreet al., 1992; Schnack-Schiel and Isla, 2005). Although the ice shelfcollapse opened space at the EAP sea surface enabling phyto-plankton blooms, the large amount of icebergs that calved fromthe ice shelves greatly reduced the available ice-free areas(personal observation), keeping the Larsen A and B bays far fromtrue open water conditions and drastically limiting primaryproduction (Arrigo et al., 2002; Arrigo and van Dijken, 2003).Lower sediment accumulation rates (SAR) values have been foundin EAP than in areas like the Northern Antarctic Peninsula, whichsimilarly to the South Eastern Weddell Sea, have not been coveredby ice shelves in the last 1000 years (Ingolfsson et al., 1998;Anderson et al., 2002; Sane et al., 2011a). In the vicinities of theSouth Shetland Islands, SAR is �3 mm yr�1 (Isla et al., 2002;Masque et al., 2002), whereas in EAP region SAR is on the order of0.4 mm yr�1 (Sane et al., 2011a). The very low SAR value in EAPsuggests that sediment accumulation is still negligible in thisregion and that only the upper millimeters of sediment corre-spond to the post-ice shelf collapse period. Differences betweenEAP and SEWS in the sediment biochemistry (Figs. 2 and 6a) maybe related to the negligible input of OM to the seafloor in Larsen

Fig. 6. MDS plot with ‘‘regions’’ as factor and with the similarity contours from the cluster analysis overlaid on the MDS plot. (a) Biochemistry data. (b) Macrofauna

abundance data. (c) Macrofauna biomass data.

E. Sane et al. / Continental Shelf Research 35 (2012) 53–63 59

before ice shelf collapses and to the still low OM input to theseafloor in EAP after Larsen A and B ice shelf disintegration in1995 and 2002, respectively. CHO are generally considered ascompounds characteristic of regions where the supply of fresh

OM is limited, like deep-sea habitats (Danovaro et al., 1993) andoligotrophic environments (Rodil et al., 2007). Furthermore, watercolumn observations showed that structural CHO concentrationincreases with depth due to the resistance of these compounds to

Table 4PERMANOVA table of results for the sediments biochemistry (a) and macrofauna

(b) data.

(a) Biochemistry data

Source of variation SS DF MS F P

Inter-region variability 281.89 1 281.89 124.18 0.001

Intra-region variability (error) 867.11 382 2.2699

Total 1149 383

(b) Macrofauna data

Source of variation SS DF MS F P(MC)

Inter-region variability 325.79 1 325.79 5.6766 0.034

Intra-region variability (error) 344.35 6 57.392

Total 670.15 7

Where: ‘‘SS’’ means ‘‘Sum of Squares’’, ‘‘DF’’ means ‘‘Degrees of Freedom’’, ‘‘MS’’

means ‘‘Mean Squares’’ and is obtained dividing the sum of squares by the degrees

of freedom, ‘‘F’’ represents the result of the F-Test and is obtained dividing the

mean squares of the inter-region variability by the mean squares of the intra-

region variability.

Table 5Results of the SIMPER test on the biochemistry data between EAP and SEWS

regions (A.S.D.: Average Squared Distance). Average similarity within regions and

dissimilarity between regions. Contribution in percentage (%) of biochemical

variables to similarity and dissimilarity.

Similarity Similarity DissimilarityEAP SEWS EAP and SEWSA.S.D. 0.22 A.S.D. 0.47 A.S.D. 1.49

LPD 37.91 LPD 77.50 LPD 77.75

PRT 33.91 CHO 13.60 CHO 13.74

CHO 28.17 PRT 8.90

Table 6Results of the SIMPER test on the relative abundance and biomass data between

EAP and SEWS regions. Average similarity within regions and dissimilarity

between regions. Contribution in percentage (%) of classes to similarity and

dissimilarity.

Similarity Similarity DissimilarityEAP SEWS EAP and SEWS

AbundanceAverage 72.59 Average 80.30 Average 28.05Polychaetes 30.53 Polychaetes 25.93 Holothuroidea 14.07

Bivalvia 13.46 Bivalvia 16.72 Pantopoda 11.64

Gasteropoda 13.33 Tunicata 12.04 Ostracoda 9.30

Tunicata 12.16 Asteroidea 9.46 Anthozoa 8.70

Asteroidea 9.42 Ostracoda 8.89 Gasteropoda 8.56

Pantopoda 7.50 Holothuroidea 8.70 Echinoidea 8.44

Porifera 5.80 Echinoidea 4.78 Bivalvia 8.16

BiomassAverage 57.64 Average 69.97 Average 42.23Polychaetes 30.35 Polychaeta 21.95 Echinoidea 13.72

Ophiurida 17.48 Holothuroidea 12.83 Porifera 9.33

Porifera 12.71 Porifera 12.35 Anthozoa 8.99

Gasteropoda 11.09 Echinoidea 12.21 Hydrozoa 8.61

Holothuroidea 8.81 Bivalvia 11.58 Holothuroidea 8.16

Hydrozoa 6.78 Ophiuroidea 9.98 Bivalvia 7.86

Bivalvia 6.15 Pantopoda 7.29 Echiurida 6.39

Table 7Results of the BEST analysis, where the variable number 1 is CHO, the variable

number 2 is PRT and the variable number 3 is LPD.

No. Var. Corr. Selections

Abundance

1 0.450 3

3 0.346 All

1 0.248 3

2 0.238 2;3

Biomass

2 0.318 2;3

1 0.275 3

1 0.163 2

3 0.053 All

E. Sane et al. / Continental Shelf Research 35 (2012) 53–6360

biological attack (Handa and Tominaga, 1969). Our results suggestthat refractory structural CHO (Liebezeit, 1984) accumulatedunder Larsen A and B ice shelves during years of ice coverageand lack of fresh OM supply, probably through lateral transport.Diatoms are protected and isolated by structural hydrophilic CHO(Hecky et al., 1973) and may represent a source of CHO. Never-theless, diatoms were absent in EAP below 2 cm depth (Sane

et al., 2011b), excluding them as sources of CHO in EAP sedi-ments. SIMPER analysis showed that, among the three biochem-ical variables studied, LPD contribute more than PRT and CHO todissimilarity between EAP and SEWS in terms of sedimentschemical composition (Table 5). The high LPD concentrations inSEWS sediment (Fig. 2) could be the result of a high input ofaggregates of diatoms (Budge and Parrish, 1998; Ramos et al.,2003), which constitute an important fraction of the vertical OMflux in the Weddell Sea (Isla et al., 2006, 2009). Zooplanktongrazing beneath sea ice also can increase LPD concentration insediments through the supply of fecal pellets (Schnack-Schiel andIsla, 2005), which concentrate LPD (phytosterols) from algae(Muhlebach and Weber, 1998). The energy content per unitcarbon of LPD is 1.4 times higher than that of CHO and 1.2 timeshigher than that of PRT (Salonen et al., 1976). Thus, SEWSsediments are characterized by OM with a high energy value thatis related to the high abundance and biomass of the macrofauna(Table 7) and maintains benthic communities also during thewinter (Isla et al., 2011). The rapid decrease of LPD concentrationsthroughout the sediment column in SEWS (Fig. 3 and Table 2)could reflect a high energetic demand by the surface depositfeeder benthic community. Marine OM is characterized by highrelative concentrations of CHO and LPD relative to PRT (Lee andWakeham, 1988). PRT are rapidly utilized by benthic organisms(Berland et al., 1970; Ittekkot, 1982; Burdige and Martens, 1988)due to the high nitrogen conversion efficiency of bacteria (Billen,1978; Newell and Field, 1983). We hypothesize that the low PRTconcentration in SEWS can be the result of a rapid consumption ofPRT by benthic organisms, whereas, in EAP, the low PRT concen-tration may reflect a still low OM input to the seafloor.

4.2. Macrofaunal community in the study area

The higher values for the abundance and the biomass of themacrofauna found in SEWS than in EAP (Table 3 and Fig. 6b and c)suggest that the development of the benthic community in EAPhas been affected by ice coverage and the consequent limitationin food supply (Grebmeier and Barry, 1991; Thomas et al., 2008).The few studies on benthos below ice shelves (Dayton and Oliver,1977; Lipps and DeLaca, 1979; Riddle et al., 2007) revealed theexistence of a variety of benthic assemblages constituted byscavengers such as amphipods (Lipps and DeLaca, 1979) and alsosuspension feeders (Riddle et al., 2007) at different depths anddistances from the ice shelf edge. These studies proposed that theobserved assemblages dwell with a low flux of OM. In the case ofthe community dominated by suspension feeders, given themagnitude of the local currents, an important lateral flux of OMwas proposed to explain the maintenance of such communities(Dayton and Oliver, 1977; Riddle et al., 2007). In the case of thepoorest environments dominated by scavengers, the assemblage

E. Sane et al. / Continental Shelf Research 35 (2012) 53–63 61

resembled those found at bathyal depths (Dayton and Oliver,1977; Lipps and DeLaca, 1979), which commonly are exposed tolimited food supply. As regards our study area, and in particularEAP region, class Demospongiae, which represents the 81% ofAntarctic sponges (McClintock et al., 2005), showed a highrelative biomass (Fig. 4b). The low growth rate of sponges(Dayton et al., 1974; Post et al., 2007) suggests that Demospon-giae lived in EAP seafloor before Larsen ice shelves disintegration(Gutt et al., 2011) and may confirm the dominance of suspension-feeding organisms, like sponges and bryozoans, under ice shelves(Riddle et al., 2007). In EAP, the relative high abundance ofTunicata, especially ascidians, typical early colonizers of icebergscours (Gutt et al., 1996), gives further evidence of the develop-ment of suspension feeder communities in the region. However,these organisms coexisted with a relatively high biomass oftypical surface deposit feeders such as Holothuroidea of thespecies Protelpidia globosa and Ophiuroidea (Fig. 4b), rapid immi-grants after iceberg scouring events (Gutt et al., 1996) adapted tolive in habitats with scarce food resources, like under ice shelves(Thomas et al., 2008). In this context, it is interesting to consider astudy on the development of the nematode community after thecollapse of the Larsen ice shelf, which evidenced that the rapidresponse of the nematofauna both in terms of abundance anddiversity, was related to the increased food availability and not toprocesses of recolonization from adjacent areas not affected bythe presence of an ice shelf (Raes et al., 2010). Our resultscorroborate that the macrobenthos response to the ice shelfcollapses is different to that of the nematodes as previouslypointed by Raes et al. (2010). Class Echinoidea showed a higherrelative biomass in SEWS than in EAP (Fig. 4b) and representedthe class, which contributed most to dissimilarity between thetwo regions in terms of macrofauna biomass (Table 6). Finally, asit occurs in benthic communities at early stages of recovery (Guttet al., 1996), the abundance and the biomass of class Polychaetawere high in EAP (Fig. 4a and b).

Only 7% of EAP seafloor showed iceberg scours (Gutt et al.,2011), suggesting that Larsen A and B were covered by floating iceshelves and, thus, that EAP benthic communities have not beenaffected by the grounding of icebergs. On the contrary, �40% to70% of SEWS bottom presented signs of iceberg disturbance (Guttand Starmans, 2001). Evident differences in the benthic commu-nity have been observed in the Antarctic continental shelfbetween areas affected by iceberg scouring and undisturbed areas(Gerdes et al., 2003). The recovery time for an Antarctic maturebenthic community has been estimated between 230 and 500years (Gutt et al., 1996; Gutt and Starmans, 2001), and benthiccommunities recovery after iceberg disturbance has beendescribed in 3 stages of succession, the first dominated by depositfeeders, the second by polychaetes and the third by suspensionfeeders like sponges and bryozoans (Gutt and Piepenburg, 2003).Due to the high abundance of iceberg scours in the Weddell Seaand the high abundance of icebergs observed off Atka Bay (Guttand Starmans, 2001; D. Gerdes, personal observation), we suggestthat iceberg scouring could represent a source of disturbance forbenthic communities in SEWS. Iceberg scouring typically impactareas shallower than 350 m depth but it may erode areas as deepas 600 m (Gutt, 2001). In SEWS, macrofauna appeared impover-ished and class Polychaeta, typical of early stages of recoloniza-tion (Gutt and Piepenburg, 2003), showed high abundance andbiomass values (Fig. 4) and was the class, which contributed mostto the intra-region similarity (Table 6). EAP and SEWS presented,in general, a similar composition of the macrofauna (Fig. 4), whichwas different from the composition of the typical benthic com-munities of the Weddell Sea (Gerdes et al., 1992; Gutt andStarmans, 2001). The narrowness of the continental shelf isresponsible for increasing currents velocity and, together with

iceberg scouring, has been invoked to explain macrofauna com-position and the exceptionally patchy spatial distributionobserved in SEWS (Gutt et al., 1998); the picture is so complexthat even recolonization processes still developing since the lastglacial retreat have been considered (Gutt et al., 1998).

The Simpson index (c) was calculated for biomass and numberof organisms per class. The Simpson index is sensitive to thedominant groups (Whittaker, 1965; Mouillot and Lepretre, 1999),and high values of the index mean dominance of one or only fewgroups. The higher Simpson index in EAP than in SEWS forabundance and biomass indicated a higher diversity in SEWSthan in EAP. High biomass sponges can increase diversity favoringthe development of epiphitic communities (White, 1984; Guttand Starmans, 1998); nevertheless, since sponges showed similarbiomasses in EAP and SEWS, we think that differences in diversitybetween the two regions should depend on other factors differentfrom sponges biomass. For example, the presence of cnidarians, inparticular of anthozoans (Fig. 4b), could have favoured, in SEWS,the formation of tridimensional structures within the suspension-feeder communities (Orejas et al., 2000), in accordance with theconcept of organisms as ecosystem engineers (Jones et al., 1994).Furthermore, the presence in SEWS of iceberg scours, which canbe from few meters to 50 m width or more (Gerdes et al., 2003),could enhance diversity in this region (Gutt et al., 1998; Pecket al., 1999; Gutt, 2001; Gutt and Piepenburg, 2003; Conlan andKvitek, 2005), in agreement with the patchy disequilibria theory(Grassle and Morse-Porteous, 1987), which suggests that moder-ate and regular disturbances can induce faunal assemblagepatchiness incrementing diversity (Pickett and White, 1985).

4.3. Sediment grain size

The 63 mm grain size limit is the physical threshold used todifferentiate fine (silt and clay) and coarse (sand and gravel)sediment. Fine sediments are usually associated with high OMcontents due to the high surface to volume ratio (Mayer, 1994),but our results showed, with the only exception of LPD concen-trations in EAP (R2

¼0.935), a poor correlation between finesediment and CHO, PRT and LPD concentrations (R2o0.331).Thus, sediment grain size in the study area cannot explain OMconcentration in the sediment column.

5. Conclusions

High concentrations of LPD were found in SEWS sedimentcolumn, while CHO showed high concentrations in EAP sedimentsmaking a difference between environments with high and lowinputs of fresh OM, respectively. LPD, CHO and PRT profiles in EAPsediment column could be related to a negligible vertical OMsupply until Larsen A and B ice shelf collapses, and a limitedvertical OM supply after Larsen ice shelves disintegration. Inaccordance with results obtained in previous works with meio-fauna (Gremare et al., 2002; Cartes et al., 2002), this studysuggests that LPD are well correlated with macrofauna abundanceand biomass, as confirmed by the statistical analysis BEST(Table 7). In spite of the higher abundance and biomass of themacrofauna in SEWS than in EAP, differences in macrofaunacomposition between the two regions were less evident. Wesuggest that iceberg scouring disturbance may in part explainthe characteristics of the macrofauna observed in SEWS, whichwas poorer than the typical rich benthic assemblages of theWeddell Sea. SEWS macrofauna composition was in fact similarto the composition of benthic communities at first stages ofrecolonization, like those present in EAP. The formation of tridi-mensional structures within the suspension-feeder communities

E. Sane et al. / Continental Shelf Research 35 (2012) 53–6362

of anthozoans, contribute to explain the higher diversity in SEWSthan in EAP.

Acknowledgments

The present work was done under the frame of the projectsANT99-1608-E (FILANT) and POL2006-06399/CGL (CLIMANT)funded by the Spanish Ministry of Science.

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