Biomass size-spectra of macrobenthic communities in the oxygen minimum zone off Chile

Estuarine, Coastal and Shelf Science 62 (2005) 217–231

www.elsevier.com/locate/ECSS

Biomass size-spectra of macrobenthic communitiesin the oxygen minimum zone off Chile

Eduardo Quirogaa,*, Renato Quinonesb, Maritza Palmab,c, Javier Sellanesb,Vıctor A. Gallardob, Dieter Gerdesd, Gilbert Rowee

aPrograma de Doctorado en Oceanografıa, Universidad de Concepcion, Departamento de Oceanografıa, Casilla 160-C, Concepcion, ChilebCentro de Investigacion Oceanografica en el Pacıfico Sur-Oriental (COPAS), Departamento de Oceanografıa,

Universidad de Concepcion, Casilla 160-C, Concepcion, ChilecPrograma de Doctorado en Ciencias Biologicas. Universidad de Concepcion, Casilla 160-C, Concepcion, ChiledAlfred-Wegener Institute for Polar and Marine Research, Columbusstrasse D-27568, Bremerhaven, Germany

eDepartment of Marine Biology, Texas A&M University, Galveston, TX 77553, USA

Received 21 November 2003; accepted 25 August 2004

Abstract

Estimates of macrofaunal secondary production and normalized biomass size-spectra (NBSS) were constructed for macrobenthiccommunities associated with the oxygen minimum zone (OMZ) in four areas of the continental margin off Chile. The presence oflow oxygen conditions in the Humboldt Current System (HCS) off Chile was shown to have important effects on the size structure

and secondary production of the benthic communities living in this ecosystem. The distribution of normalized biomass by size waslinear (log2–log2 scale) at all stations. The slope of the NBSS ranged from �0.481 to �0.908. There were significant differencesbetween the slopes of the NBS-spectra from the stations located in the OMZ (slopeZ�0.837) and those located outside the OMZ

(slopeZ�0.463) ( p! 0.05). The results of this study suggest that low oxygen conditions (!0.5 ml L�1) appear to influence biomasssize-spectra, because small organisms are better able to satisfy their metabolic demands. The annual secondary production washigher off central Chile (6.8 g Cm�2 y�1) than off northern Chile (2.02 g Cm�2 y�1) and off southern Chile (0.83 g Cm�2 y�1). A

comparison with other studies suggests that secondary production in terms of carbon equivalents was higher than in other upwellingregions.� 2004 Elsevier Ltd. All rights reserved.

Keywords: macrobenthos; biomass size-spectra; oxygen minimum zone; off Chile

1. Introduction

Oceanic oxygen minimum zones (OMZs) are ubiqui-tous and persistent features on the eastern continentalmargins of ocean basins, where dissolved oxygenconcentrations decrease to low levels (!0.5 ml L�1;Kamykowski and Zentara, 1990). These OMZs develop

* Corresponding author.

E-mail address: [email protected] (E. Quiroga).

0272-7714/$ - see front matter � 2004 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2004.08.020

beneath highly productive surface waters associatedwith upwelling and result from the depletion of oxygenin the water column due to high biological and biochem-ical demand (Wyrtki, 1962; Rowe, 1981). OMZs inter-cept the continental margin producing strong gradientsof bottom-water dissolved oxygen and organic matterinput (Levin et al., 2000), and unique biogeochemicalprocesses (Karl and Knauer, 1984; Smith et al., 2000).The vertical distribution of benthic populations andcommunity structure are greatly influenced by the pre-sence of OMZs (Menzies et al., 1973; Rosenberg et al.,

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218 E. Quiroga et al. / Estuarine, Coastal and Shelf Science 62 (2005) 217–231

1983; Wishner et al., 1990; Arntz et al., 1991; Levinet al., 1991, 2000; Neira et al., 2001). Benthic faunaof the OMZs is generally dominated by nematodes,oligochaetes and small-bodied polychaetes, probablyassociated to the high availability of food and thereduction in predation pressure (Levin et al., 2002).

In the HCS a pronounced OMZ is associated with theEquatorial subsurface water (ESSW), which flows pole-ward over the shelf and upper slope (Silva and Neshyba,1979). This extensive water mass produces a large regionwith oxygen depletion, extending at least from 50 to400 m depth in northern Chile with concentrations!0.5 ml L�1 (Morales et al., 1999). In central Chile theOMZ continues to be a significant feature extending inwinter from 100 to 300 m (Gallardo et al., 1995). Earlystudies on benthic communities on the shelf and upperslope in northern Chile suggested that low oxygenconcentrations within the water column had importanteffects on the benthic biomass (Gallardo, 1963). Fur-thermore, it is known that the OMZ of the HCSrepresents an important barrier to aerobic metabolicprocesses (Eissler and Quinones, 1999), leading to di-verse questions about responses of the fauna to hypoxicconditions.

Many authors have stressed the importance of bodysize in benthic marine fauna, but very little is knownabout the processes that determine size distribution inmarine invertebrates (Roy, 2002). Studies have focusedon bathymetric patterns in relation to the availability offood (Thiel, 1975, 1979), physiological and ecologicalfactors (Rex and Etter, 1998), or phylogenetic con-straints (Rex et al., 1999). More recently, Chapelle andPeck (1999) and McClain and Rex (2001) proposed thatmaximum body size in benthic marine invertebrates is afunction of the availability of dissolved oxygen concen-trations. This hypothesis is related directly to physio-logical effects of oxygen concentration on invertebrates,although other factors, such as life history, may beinvolved (Peters, 1983). Studies dealing with the effect ofenvironmental factors on body size distribution oforganisms in marine benthic communities are scarce.The physical characteristics of the sediment (Schwing-hamer, 1981; Drgas et al., 1998; Duplisea, 2000), thegradient of organic matter (Schwinghamer, 1988), or thelife-history strategies of dominant taxa (Warwick, 1984)are thought to constrain the size-spectrum of infaunalspecies. However, attempts to relate the effects of dis-solved oxygen with the macrofaunal biomass size-spectra(BSS) are scarce (Drgas et al., 1998; Gonzalez-Oreja andSaiz-Salinas, 1999) and thus results are not conclusive.

The smaller size classes are important componentsof benthic communities in upwelling areas of the HCS(Rowe, 1971a). According to Peters (1983), communitiesdominated by smaller individuals may have higher pro-ductivity/biomass ratios and thus influence energy flowand nutrient processing. Despite the importance of the

HCS there is very little data on benthic secondaryproduction and the factors that control it, althoughsome of the estimates in this area are among the highestever reported (Rowe, 1985).

Due to logistic constraints, quantitative macro-benthic studies in the area have traditionally focusedon the shelf off central (e.g. Gallardo et al., 1995;Carrasco et al., 1999; Gutierrez et al., 2000) and northernChile (Gallardo, 1963; Ramorino and Muniz, 1970;Zuniga et al., 1983; Carrasco, 1997; Quiroga et al., 1999).Recently, benthic surveys have been extended onto thecontinental slope (Gallardo et al., 2004; Palma et al., inpress).

Despite the advances in the understanding of thefunction and structure of benthic communities in theHCS achieved during the last two decades, no quanti-tative studies on the BSS of benthic communities in thisregion have been conducted to date. In this context, thispaper aims (1) to analyze the density, biomass and BSSof the benthic macrofauna living on the continentalmargin off Chile; (2) to determine the influence of theOMZ on the BSS of the benthic macrofauna; and (3) toestimate macrofauna secondary production from P/Bratios for the whole community.

2. Materials and methods

2.1. Field sampling

The study area is the continental margin off Chile(Fig. 1). Five cruises were conducted in this areabetween 1999 and 2001 (see Table 1). The surveyswere carried out off Iquique (21 � Lat.S), off Antofagasta(22 � Lat.S), off Concepcion (36 � Lat.S), and off Chiloe(42 � Lat.S), covering a depth range from 100 to 2000 m.

Amini-multiple corer with six tubes (inner diameterZ95 mm) was used to collect the samples (Barnett et al.,1984). At each station, two to four multicorer dropswere conducted. From each of the multicore drops, oneto four cores were analyzed. Sediments were sieved ondeck through a 300 mm mesh and preserved in buffered10% sea-water solution of formaldehyde. In thelaboratory the specimens were transferred to a 70%ethanol solution. All macrofauna samples were sortedin the laboratory using a dissecting microscope. Theindividuals were weighed wet and this value was con-verted to dry mass and kiloJoule using standard con-version factors published by Brey (2001). At eachstation, water column temperature, salinity and dis-solved oxygen were measured using a CTDO. In addi-tion, dissolved oxygen (DO) measurements were madeusing a semi-automatic version of the Winkler method(Williams and Jenkinson, 1982) based on a photometricend-point detector, a Dosimat 665 (Metrohom) and

219E. Quiroga et al. / Estuarine, Coastal and Shelf Science 62 (2005) 217–231

710671077102

7103 7104

7175

7160

7174 7177

7173

7172

71617167

7163

71627166

75° 73°44°

42°

40°

38°

36°

75° 73°

SouthAmerica

35 4

16

2

1

2

3

4

AB

CD

A

B

C D

73°73°70°

36°

20°

21°

40°

20°

0°

70°270°7

23°4

22°9

Fig. 1. Positions of sampling stations on the continental margins of Chile. MinOx Expedition (A), PUCK Expedition (B and D), Thioploca-Chile

Expedition (C).

a chart recorder. The analytical procedures wereconducted as suggested by Knap et al. (1993).

Chlorophyll-a (Chl-a) and phaeopigments (Phaeop)were analyzed photo-spectrometrically according to Stalet al. (1984). The sum of Chl-a and Phaeop is consideredas chloroplastic pigment equivalent (CPE). Total organiccontent of surface sediments (TOC) and C/N ratios werekindly supplied by the geological working group of theUniversity of Bremen. Sediment grain analysis was per-formed using geological sieves according to Buchananand Kain (1971). Particle size data were analyzed fol-lowing Folk (1974).

2.2. Data analysis

The density and biomass data from each core-replicatewere standardized by area and then used to determinethe means and standard deviations per stations. Addi-tionally, mean individual weight (W ) was estimated astotal macrofauna community biomass divided by totalmacrofauna community density. Analyses of varianceand a posteriori Tukey’s HSD test (Sokal and Rohlf,1981) were performed to estimate the presence ofsignificant differences in the density and biomass

of the macrofauna organisms analyzed as a function ofgeographic location, depth and dissolved oxygen level(i.e. OMZ stations versus non-OMZ stations).

Biomass size-spectra were normalized (NBSS) asdescribed by Platt and Denman (1977, 1978). This norm-alization is required since the width of the size classesvaries through the size-spectra. In brief, the procedureconsists of dividing the variable of interest m(s) in thesize class characterized by the weight or volume (s) bythe width of the size class, Ds. Thus the normalizedversion of the variable m is equal to:

MðsÞZmðsÞ=Ds

The parameters of the NBSS were determined byregressing the log2 (normalized biomass) against log2(individual weight). The slopes of NBSS were comparedaccording to Zar (1984). The spectra were constructedwith a maximum of 11 size classes.

The amount of uncertainty which exists regarding thesize class to which a unit of biomass selected at randombelongs is defined as the biomass size diversity (BSDIV)(Quinones, 1992). The greater the uncertainty, thegreater is the diversity (Pielou, 1966). We have used


Table 1

List of sampling sites on the continental margin off Chile, geographical position, water depth, and number of the samples

Location Expedition Vessel Date Station Water

depth (m)

Latitude

( �S)

Longitude

( �W)

No. of

drops

No. of

cores examined

Iquique MinOx R/V Vidal Gormaz 30.03.2000 St 1 111 20 �14#07 70 �12#04 4 6

31.03.2000 St 2 204 20 �16#36 70 �13#98 3 3

01.04.2000 St 3 300 20 �16#84 70 �14#88 4 5

02.04.2000 St 4 517 20 �15#50 70 �17#24 4 4

03.04.2000 St 5 840 20 �16#73 70 �28#21 4 4

04.04.2000 St 6 1278 20 �13#40 70 �38#15 4 4

Antofagasta PUCK R/V Sonne 01.04.2001 7102 142 22 �49#59 70 �28#29 2 3

02.04.2001 7104 295 22 �51#96 70 �29#39 2 6

04.04.2001 7107 518 22 �50#50 70 �30#93 2 6

02.04.2001 7103 890 22 �51#99 70 �32#58 3 8

04.04.2001 7106 1350 22 �47#98 70 �32#58 3 8

Concepcion ETC R/V Vidal Gormaz 29.03.1999 St 1 120 36 �26#06 73 �23#24 4 12

30.03.1999 St 2 206 35 �44#60 73 �04#41 3 8

04.04.1999 St 3 364 36 �02#31 73 �04#22 4 11

05.04.1999 St 4 810 36 �32#70 74 �04#90 3 8

Concepcion PUCK R/V Sonne 23.04.2001 7161 124 36 �25#52 73 �23#36 3 7

23.04.2001 7160 365 36 �02#35 73 �04#40 3 7

24.04.2001 7163 535 36 �25#49 73 �35#72 3 7

24.04.2001 7162 798 36 �32#54 73 �40#05 3 9

25.04.2001 7166 1294 36 �27#99 73 �46#47 3 9

26.04.2001 7167 2060 36 �27#17 73 �54#18 2 6

Chiloe PUCK R/V Sonne 39.04.2001 7173 160 42 �05#36 74 �33#55 2 6

39.04.2001 7172 297 42 �24#61 74 �47#26 2 4

03.05.2001 7177 902 42 �34#96 74 �50#22 3 7

01.05.2001 7174 1224 42 �32#66 75 �01#10 3 7

01.05.2001 7175 1961 42 �27#13 75 �12#61 3 8

the following size diversity index proposed by Ruiz(1994):

HcjZ� ð1=log2 NÞX

ðci=RÞðbi=BÞlog2ðbi=BÞ

where ci is the width of size class i, R is the width of thetotal size range analyzed, bi is the biomass of size class i,B is the biomass of the total size range analyzed, and Nis the number of size classes. This Hc index, which is amodification of the Shannon index of diversity (Marga-lef, 1957), takes into consideration the fact that biomassspectra usually do not have size classes with equal width.Accordingly, each class has a weight factor (i.e. ci/R).The Hc index (analogous to Shannon’s species diversityindex) will have its minimum value (HcZ 0) when allbiomasses in the sample belong to only one size class.The Hc index will be maximum when the biomass isequally distributed among the size classes in the sample.The jackknifing analytical procedure was used toprovide bias and variance (Hcj) (Magurran, 1988).

Annual production/biomass (P/B) ratio and second-ary production (P) were estimated using the artificialneural network (ANN) model proposed by Brey et al.(1996).

Correlation between community/population variables(i.e. densities, biomass, individual weight, productionand normalized biomass size-spectrum parameters)

and environmental variables (i.e. depth, dissolved oxy-gen, sediment-bounded pigments, TOC and C/N ratio)were calculated using Pearson’s correlation analysis.The community/population variables and environ-mental variables were logarithmically transformed aslog10(XC 1).

3. Results

3.1. Dissolved oxygen

Results of bottom-water dissolved oxygen measure-ments are shown in Fig. 2. Values of oxygen at Iquiquewere lowest, ranged from 111 m to 300 m (0.24 ml L�1)and began to increase at 517 m, defining the base ofthe OMZ (0.97 ml L�1). Higher values of oxygen wereobserved at 840 and 1278 m stations (O1.39 ml L�1).Off Antofagasta, the lowest near bottom oxygen levelswere recorded on the shelf in 142 and 295 m water depth(0.05 and 0.06 ml L�1, respectively), hereafter defined asthe OMZ. Oxygen levels increased with depth, reaching0.9 ml L�1 on the upper slope (518 m depth) and thehighest values at the lower-slope sites in 900 and 1350 mwater depth with 1.3 and 1.7 ml L�1, respectively.


During 1999, values of DO off Concepcion werelowest in 120 and 206 m depth (!0.13 ml L�1) andhighest at 810 m (2.98 ml L�1). At the 364 m station aDO concentration of 0.52 ml L�1 was observed. During2001, in the same area, low saturation levels occurredexclusively in 124 m water depth (0.45 ml L�1), whereasin 365 m water depth the critical 0.5 ml L�1 value hasalready exceeded, which normally characterizes OMZareas. At 535 m a maximum of 2.92 ml L�1 occurredand with increasing depth the saturation decreasedslightly to 1.5 and 1.8 ml L�1 in 1300 and 2000 m depth,respectively. Off Chiloe the oxygen levels near thebottom varied between 1.3 ml L�1 in 160 m water depthto a maximum of 2.8 ml L�1 in 500 m on the upperslope. The OMZ off northern Chile was thicker and wasabsent off Chiloe. Nevertheless the oxygen levels offChiloe still reflected the influence of the ESSW (Silvaand Neshyba, 1979).

3.2. Sediment analysis

The sediments off Iquique presented a more variablecontent of silt-clay with the deepest stations havinglower percentages (Table 2). The sediments off Antofa-gasta appeared quite heterogeneous with higher percen-tages of sand at the 142 m, 518 m, and 1350 m stations(O94%). In contrast, the sediments at the sampling sitesoff Concepcion were dominated by the mud fraction and

0

200

400

600

800

1000

1200

1400

1600

1800

2000

2200

0 1 2 3 4 5 6Dissolved oxygen (ml L-1)

Wat

er d

epth

(m)

Iquique ( MinOx)Antofagasta ( PUCK)Concepción ( ETC)Concepción ( PUCK)Chiloé ( PUCK)

Fig. 2. Water column dissolved oxygen profiles in the study area.

sand made up, with the exception of the 535 m station(27.48%), less than 5%. Off Chiloe, sediments at the twoshelf stations contained between 41 and 55% mud,whereas the lower-slope stations were dominated bymud and sand made up less than 2%.

Sediment-bounded pigments mainly Phaeop, rangedfrom low value of 39.18 mg g�1 at 840 m to highest valueof 868.83 mg g�1 at 204 m off Iquique (Table 2). Chl-a,a measure of fresh organic matter, ranged from 8.57to 98.88 mg g�1 and represent about 10% of the totalpigment content (CPE). Off Antofagasta, Phaeop variedranging from a low value of 20.70 mg g�1 at 1350 mto a high value of 49.09 mg g�1 at 518 m. Off Concep-cion Phaeop ranged from 18.19 mg g�1 at 535 m to74.96 mg g�1 at 124 m, and Chl-a ranged from 2.31 to10.33 mg g�1 during 1999. In contrast, during 2001 offConcepcion highest values of Phaeop were observed,ranging from 126.6 to 277.7 mg g�1 and Chl-a from 12.92to 35.67 mg g�1. Off Chiloe lowest values of Chl-a,Phaeop and CPE were observed. Phaeop varied between12.53 mg g�1 at 160 m and 21.90 mg g�1 at 902 m depth.

3.3. Macrofaunal densities, biomass and production

The densities and biomasses of the macrofaunaexhibited significantly higher values off Concepcion incomparison to those from Iquique, Antofagasta andChiloe (F4,74Z 14.4, p! 0.001) (Fig. 3 and Table 3). OffIquique the density and biomass were highest at the517 m station (meanG S.D.) (14 531G 9091 ind m�2,28.78G 25.99 g wet wt m�2) and lowest at the 204 mstation (188G 81 ind m�2, 0.19G 0.06 g wet wt m�2).Off Antofagasta density and biomass were highest atthe 142 m station (14 718G 3286 ind m�2, 13.78G 3.87 gwet wt m�2) and lowest at the 1351 m station (2879G866 ind m�2, 1.93G 0.86 gwet wt m�2). Tukey’s analysesshowed significant differences for density and biomasswhen comparing the 1351 m station with those locatedon the shelf ( p! 0.01). Off Concepcion, the density washighest at the 206 m station (21 036G 8676 ind m�2)and lowest at the 364 m station (9117G 2178 ind m�2).Biomass was highest at the 810 m station (69.9G 23.43 gwet wt m�2) and lowest at the 206 m station (19.16G6.84 g wet wt m�2). In the same area, during 2001, offConcepcion the macrofauna densities and biomasseswere highest at the 124 and 535 m stations (30 837G3171 ind m�2, 96.28G 29.71 g wet wt m�2, and 34 405G8480 ind m�2, 52.26G 20.64 g wet wt m�2), and lowest atthe 2060 m station (6355G 224 ind m�2, 5.82G 2.37 gwet wt m�2, p! 0.001). Density and biomass dif-fered significantly among shelf and lower-slope stations(F9,21Z 10.95, p! 0.01). ANOVA analyses showedsignificant differences for density between stations locatedin the OMZ and those located outside the OMZ(p! 0.01).


Table 2

List of sediment parameters on the continental margin off Chile, dissolved oxygen (DO), percentage of mud, chlorophyll-a (Chl-a), phaeopigment

(Phaeop), chloroplastic equivalent pigments (CPE), percentage of total organic carbon (TOC) and C/N ratio

Location (Expedition) Station Depth (m) DO (ml L�1) % Mud mg Chl-a g�1 mg Phaeop g�1 CPE (mg g�1) TOC (%) C/N

Iquique (MinOx) St 1 111 0.24 55.40 50.19 359.53 409.72 – –

St 2 204 0.24 90.90 98.88 769.95 868.83 – –

St 3 300 0.24 92.40 61.95 472.66 534.61 – –

St 4 517 0.97 61.80 18.50 126.36 144.86 – –

St 5 840 1.39 40.80 8.57 39.18 47.75 – –

St 6 1278 1.98 42.40 19.68 97.68 117.36 – –

Antofagasta (PUCK) 7102 142 0.05 0.53 4.83 35.66 40.48

7104 295 0.06 73.78 4.61 33.65 38.26 4.80 7.76

7107 518 0.90 5.53 7.35 49.09 56.44 – –

7103 890 1.28 74.11 3.40 28.13 31.53 4.99 8.06

7106 1350 1.70 2.03 2.58 20.70 23.28 3.14 8.15

Concepcion (ETC) St 1 120 0.10 99.50 35.67 277.7 313.37 4.26 8.50

St 2 206 0.13 97.90 12.92 126.6 139.52 1.13 7.63

St 3 364 0.52 99.60 13.26 131.3 144.56 3.06 8.73

St 4 810 2.89 98.70 13.36 150.9 164.26 2.13 8.38

Concepcion (PUCK) 7161 124 0.45 98.75 10.33 74.96 85.29 4.28 7.26

7160 365 0.79 97.76 3.56 26.35 29.91 2.97 7.89

7163 535 2.92 72.52 2.31 18.19 20.50 2.06 7.86

7162 798 2.30 95.69 4.08 21.53 25.61 2.61 7.96

7166 1294 1.48 96.93 2.83 24.33 27.16 3.08 7.92

7167 2060 1.82 98.33 3.48 28.37 31.85 3.04 7.73

Chiloe (PUCK) 7173 160 1.28 41.14 1.50 12.53 14.03 1.34 8.31

7172 297 1.52 54.57 1.23 12.83 14.06 1.56 8.89

7177 902 2.31 98.22 2.50 21.90 24.40 3.53 8.60

7174 1224 1.87 98.81 2.07 19.13 21.20 3.40 8.02

7175 1961 1.93 98.05 1.65 16.15 17.81 3.12 10.19

0

200

400

600

800

1000

1200

1400

1600

1800

2000

2200

0 5000 10000 15000 20000 25000 30000 35000 40000 45000Mean densities (ind m-2)

Wat

er d

epth

(m)

Iquique (MinOx)Antofagasta (PUCK)Concepcion (ETC)Concepcion (PUCK)Chiloe (PUCK)

Fig. 3. Mean density (Gstandard error) of benthic macrofauna

sampled in the study area.

The macrobenthic densities off Chiloe were highest atthe 297 m station (7042G 398 ind m�2) and lowest atthe 1961 m station (3090G 965 ind m�2, Fig. 3), al-though an a posteriori Tukey test revealed no significantdifferences among the stations ( pO 0.05). Biomass washighest at the 902 m station (16.20G 10.54 g wetwt m�2) and lowest at the 160 m station (7.83G 5.22 gwet wt m�2), but did not differ significantly amongstations ( pO 0.05).

Total secondary production estimates for macro-benthos reflected the spatial variability in densitiesand biomass among locations and stations across theshelf and continental slope. Total production washigher of Concepcion (65.22G 72.05 g wet wt m�2 y�1)as compared to that off Iquique (18.89G 20.83 gwet wt m�2 y�1), off Antofagasta (25.14G 26.36 gwet wt m�2 y�1) and off Chiloe (15.67G 4.74 g wetwt m�2 y�1) (Table 3). Polychaetes secondary produc-tion contributed most to benthic production (about90%) at all study sites (i.e. Antofagasta, Concepcion,Chiloe) except Iquique. In the latter, peracarid crusta-ceans (amphipods) contributed most to secondary pro-duction at Iquique (55%).

The P/B ratio of the macrofaunal community wasabout 2.7 y�1. This value is close to that reported byCarrasco and Arcos (1980, 1984) based on the cohortsummation method for Paraprionospio pinnata (2.4 y�1)


Table 3

Macrofaunal biomass and secondary production at the stations on the continental margin off Chile

Location Station Depth Total macrofauna Polychaetes and oligochaetes Crustaceans Molluscs

(m) Mean S.D. Mean S.D. Mean S.D. Mean S.D.

(A) Biomass (g wet wt m�2)

Iquique (MinOx) St 1 111 12.099 21.215 0.453 0.429 11.646 21.368

St 2 204 0.198 0.065 0.198 0.065

St 3 300 3.453 4.861 3.340 4.642 0.113 0.225

St 4 517 28.784 25.993 17.873 2.016 5.919 2.502 1.989 0.870

St 5 840 3.859 2.805 2.208 0.196 0.077 0.007 1.567 1.058

St 6 1278 8.631 10.947 2.489 0.334 0.363 0.123 5.810 3.315

Mean 9.504 4.427 3.624 3.122

S.D. 10.337 6.698 5.127 2.337

Antofagasta (PUCK) 7102 142 13.785 3.879 9.559 2.096 3.813 5.393 0.412 0.582

7104 295 12.211 0.591 12.155 0.511 0.056

7107 518 12.493 11.905 5.237 1.908 0.305 0.239 6.951 9.756

7103 890 5.297 1.470 3.457 0.343 0.496 0.765 1.273 1.025

7106 1351 1.937 0.862 1.573 1.064 0.184 0.117 0.129 0.119

Mean 9.145 6.396 0.971 2.191

S.D. 5.218 4.371 1.597 3.210

Concepcion (ETC) St 1 120 60.847 40.131 53.494 41.337 6.541 2.565 0.122 0.129

St 2 206 19.159 6.842 17.840 6.675 0.507 0.794

St 3 364 44.039 42.740 32.848 35.402 6.063 8.654 1.466 1.471

St 4 810 69.902 23.428 41.103 15.475 0.939 0.987 25.192 14.394

Mean 48.487 36.321 3.513 8.927

S.D. 22.296 14.960 3.232 14.102

Concepcion (PUCK) 7161 124 96.286 29.714 79.713 18.974 10.613 6.318 5.956 4.789

7160 365 41.439 22.529 40.185 22.162 0.191 0.254 0.504 0.154

7163 535 52.259 20.643 42.229 20.069 0.261 0.208 9.686 1.376

7162 798 41.469 25.458 30.392 19.826 0.148 0.076 10.330 6.095

7166 1294 22.615 11.275 21.505 11.946 0.274 0.278 0.500 0.339

7167 2060 5.820 2.374 4.198 1.206 0.325 0.431 1.296 0.736

Mean 43.315 36.370 1.969 4.712

S.D. 30.748 25.374 4.235 4.582

Chiloe (PUCK) 7173 160 7.837 5.217 5.895 4.632 1.195 0.545 0.783 0.535

7172 297 10.683 7.330 8.165 7.444 1.595 1.060 0.859 0.856

7177 902 16.201 10.540 6.549 7.330 0.617 0.492 1.091 1.208

7174 1224 11.226 10.831 10.360 10.705 0.341 0.130 0.371 0.154

7175 1961 12.256 6.772 5.236 3.338 0.276 0.164 3.105 2.745

Mean 11.641 7.241 0.805 1.242

S.D. 3.030 2.055 0.572 1.073

(B) Production (g wet weight m�2 y�1)

Iquique (MinOx) St 1 111 38.629 15.627 2.559 0.719 36.070 21.245

St 2 204 0.873 0.254 0.873 0.254

St 3 300 12.095 5.578 11.753 6.471 0.342 0.000

St 4 517 51.181 3.249 30.419 2.379 15.513 6.673 1.257 0.483

St 5 840 4.523 0.294 3.639 0.305 0.132 0.017 0.752 0.484

St 6 1278 6.051 0.527 3.263 0.344 0.399 0.108 2.332 1.299

Mean 18.892 8.751 10.491 1.447

S.D. 20.853 11.271 15.746 0.807

Antofagasta (PUCK) 7102 142 55.057 5.123 47.974 5.948 6.069 3.002 1.014 0.258

7104 295 50.357 10.508 50.172 11.002 0.185 0.000

7107 518 10.542 0.926 6.826 0.689 0.689 0.193 2.875 1.338

7103 890 7.032 0.224 5.435 0.242 0.553 0.173 0.936 0.190

7106 1350 2.731 0.124 2.272 0.136 0.287 0.156 0.114 0.019

Mean 25.144 22.536 1.556 1.235

S.D. 25.368 24.294 2.530 1.167

Concepcion (ETC) St 1 120 111.386 7.452 104.366 8.370 5.933 3.048 0.272 0.123

St 2 206 44.475 2.400 42.406 2.666 0.699 0.265

St 3 364 51.825 2.731 43.911 3.303 4.171 0.648 1.099 0.215

(continued on next page)


Table 3 (continued)

Location Station Depth Total macrofauna Polychaetes and oligochaetes Crustaceans Molluscs

(m) Mean S.D. Mean S.D. Mean S.D. Mean S.D.

St 4 810 52.030 5.434 39.873 7.071 1.764 0.363 8.828 3.558

Mean 64.929 57.639 3.142 3.400

S.D. 31.170 31.196 2.360 4.719

Concepcion (PUCK) 7161 124 206.436 16.170 189.607 17.913 10.626 0.000 6.194 0.924

7160 365 52.763 2.550 50.692 2.779 0.460 0.065 0.582 0.223

7163 535 62.607 3.921 54.359 4.289 0.720 0.394 7.393 2.071

7162 798 40.211 2.763 34.549 3.132 0.318 0.096 4.839 1.676

7166 1294 22.349 1.076 21.314 1.251 0.355 0.067 0.392 0.060

7167 2060 6.968 0.366 5.606 0.412 0.527 0.238 0.835 0.147

Mean 65.222 59.355 2.168 3.373

S.D. 72.056 66.358 4.146 3.143

Chiloe (PUCK) 7173 160 19.359 0.903 14.127 0.989 3.910 0.932 1.313 0.290

7172 297 20.243 0.838 15.002 0.853 4.159 1.165 1.007 0.130

7177 902 17.206 0.718 8.672 0.508 1.074 0.205 0.738 0.204

7174 1224 12.369 0.869 11.274 1.025 0.594 0.141 0.318 0.074

7175 1961 9.171 0.303 5.890 0.257 0.284 0.048 1.372 0.224

Mean 15.670 10.993 2.004 0.950

S.D. 4.744 3.788 1.877 0.435

and the amphipod Ampelisca araucana (3.6 y�1), whichare the most dominant species in the benthic assemb-lages of the continental shelf off central Chile (Gallardoet al., 1995).

3.4. Normalized biomass spectra

Normalized biomass spectra were constructed forgroups of stations pooled according to depth ranges(Table 4). Most NBSS were statistically significant

(p! 0.05) presenting slopes ranging from �0.481 to�0.908 (Table 4). No significant differences (p! 0.05)were found among the slopes of the NBSS when compar-ing different depth ranges as well as among locations.

Pooling together spectra of all locations, disregardingthe water depth, all NBSS can be represented by the log–log linear model (p! 0.05, Table 4). No significantdifferences were found among the slopes of the NBSS(Table 4). However, and as expected from the differentlevels of benthic biomass found between Concepcion and

Table 4

Regression parameters for the normalized biomass size-spectra of the stations on the continental margin off Chile (Model: log2YZlog2 aC b log2X )

Location Depth range (m) Slope Log2 a r2 N Std. error slope Std. error log2 a p value

Iquique (MinOx) 100–300 �0.952 1.855 0.33 6 0.956 1.482 pO 0.05

300–1000 �0.687 2.354 0.62 8 0.221 0.693 p! 0.05

1000–2000 �0.291 0.938 0.41 5 0.199 0.551 pO 0.05

Combined depth �0.475 2.001 0.48 8 0.203 0.637 p! 0.05

Antofagasta (PUCK) 100–300 �0.956 3.088 0.56 6 0.419 1.144 pO 0.05

300–1000 �0.481 1.547 0.76 9 0.103 0.426 p! 0.01

1000–2000 �0.706 1.246 0.91 6 0.113 0.296 p! 0.001

Combined depth �0.685 2.593 0.81 9 0.124 0.512 p! 0.001

Concepcion (ETC) 100–300 �0.908 4.785 0.74 9 0.201 0.741 p! 0.01

300–1000 �0.299 2.087 0.20 10 0.213 0.905 pO 0.05

1000–2000 – – – – – – –

Combined depth �0.569 4.268 0.77 10 0.110 0.467 p! 0.001

Concepcion (PUCK) 100–300 �0.848 5.038 0.69 10 0.202 0.926 p! 0.01

300–1000 �0.351 2.385 0.35 11 0.158 0.758 pO 0.05

1000–2000 �0.777 3.293 0.81 9 0.145 0.536 p! 0.01

Combined depth �0.611 4.097 0.87 11 0.079 0.378 p! 0.001

Chiloe (PUCK) 100–300 �0.742 2.284 0.77 9 0.151 0.588 p! 0.01

300–1000 �0.502 2.037 0.49 9 0.194 0.716 p! 0.01

1000–2000 �0.537 2.290 0.74 10 0.112 0.475 p! 0.01

Combined depth �0.565 2.427 0.85 10 0.084 0.356 p! 0.01

Size range: 0.01–512 mg wet wt. Depth range: 111–2060 m.


the rest of the locations, the intercept of the NBSSof this location was significantly different from the otherlocations (p! 0.05, Table 4). It is known that the in-tercept of NBSS is an indicator of total biomass of thesystem (Sprules and Munawar, 1986; Quinones et al.,2003).

For comparative purposes NBSS data were pooledtogether from all stations located in the OMZ andoutside the OMZ (Fig. 4). Both regression models werehighly significant ( p! 0.001) and residual variationswere small. The slope of the NBSS for organisms livingin the OMZ (�0.837) was significantly different (p!0.05) from that of organisms living beneath OMZ(�0.463). This indicates that benthic communities inha-biting the OMZ consist of smaller macrofauna in com-parison to the size-structures observed at stationslocated beneath the OMZ.

Finally, Fig. 5 shows the NBSS constructed withall data collected. The spectra fit with a log2–log2 linearmodel having a slope of �0.559. The slope does notchange significantly when the data from Chiloe, i.e. theonly location located on the southern edge of theHCS without a pronounced OMZ, are excluded (i.e.slopeZ�0.555, interceptZ 3.228, r2Z 0.60).

3.5. Biomass size diversity

The BSDIV reflected low values for the OMZ stations(Fig. 6), where only few size classes were observed. Innorthern Chile the BSDIV was lowest in the 204 and295 m stations. The highest BSDIV was found at the 365and 518 m stations off Antofagasta and Concepcion,respectively. Off Chiloe the BSDIV was highest at the160 m and lowest at the 297 and 1224 m stations.

3.6. Correlations between abiotic andbiotic parameters

A Pearson correlation analysis was performed withthe most relevant parameters (Table 5), i.e. water depth,dissolved oxygen, % mud, sediments-bounded pigments,total organic carbon, C/N ratio, versus total densities,biomass and secondary production of macrofauna, para-meters (slopes and intercepts) of the NBSS, and biomasssize diversity. The analysis (pairwise selection) wascarried out for 26 stations on the five transects.

Significant correlations ( p! 0.05) were found be-tween depth and total density of macrofauna, totalbiomass of polychaetes and crustaceans, secondary pro-duction of total macrofauna, polychaetes and crusta-ceans (Table 5). Dissolved oxygen was positivelycorrelated with the slope of NBSS. Chl-a, Phaeop andCPE were positively correlated with total biomass andsecondary production of macrofauna. Chl-a was alsopositively correlated with the intercept of NBSS. Incontrast, individual weight, total biomass and pro-duction of molluscs and biomass size diversity showedalmost no correlation with abiotic parameters chosenfor this analysis.

4. Discussion

4.1. Environmental setting

The sediment-bounded pigment content measured inthis study was in the same order of magnitude as thosereported by Gutierrez et al. (2000) on the shelf offcentral Chile (9–482 mg g�1), and Levin et al. (2000) on

y = -0.837x + 4.673r2 = 0.81

-4

0

4

8

-4 -2 0 2 4 6 8 10

A

-2

-1

0

1

2

-4 -2 0 2 4 6 8 10

B

y = -0.463x + 2.746r2 = 0.80

-4

0

4

8

-4 -2 0 2 4 6 8 10

C

-2

-1

0

1

2

-4 -2 0 2 4 6 8 10

D

Log 2

(bio

mas

s/∆

wei

ght)

Log 2

(bio

mas

s/∆

wei

ght)

Log2 size -class

Log2 size-class

Log2 size-class

Log2 size-class

Stan

dard

ized

resi

dual

s

Stan

dard

ized

resi

dual

s

Fig. 4. Normalized biomass size-spectra and residuals distribution of the macrofauna in the OMZ (A and B) and outside OMZ (C and D) stations.


the shelf and slope on the Oman margin, NW Arabiansea (68–770 mg g�1), but our values were higher thanthose reported by Levin et al. (2002) for the OMZ offPeru (10.5–99.4 mg g�1). C/N ratios appeared homoge-neous, without showing any relation to water depth andranged from 7.26 to 10.19. These values were similar tothose reported by Hebbeln et al. (2000) for central Chile(30 �S). The sediment-bounded pigment content andC/N ratios confirm that the sediments associated withupwelling areas off Chile are rich in organic matter.The TOC values determined in this study were also inthe same range as those reported by Thandrup andCandfield (1996) for the shelf areas off central Chile.

4.2. Macrofaunal densities, biomass and production

The standing stock of macrofauna organisms wascomparable to or slightly higher than those found duringprevious studies on the shelf off central Chile (e.g.Gallardo et al., 1995; Carrasco et al., 1999; Gutierrezet al., 2000). Standing stock was also generally higherthan from stations located in the upper and lower slopeareas along the Chilean coast. Overall densities andbiomasses tended to decline at depths greater than500 m, this pattern does not appear to be influenced bythe presence of the OMZ. In fact, Gallardo et al. (2004)and Palma et al. (in press) reported higher densitiesand biomasses in the OMZ and beneath the OMZ(upper slope). It is well documented that macrofaunal

y = -0.559x + 3.066r2 = 0.63

-4

0

4

8

-4 -2 0 2 4 6 8 10

-3

-2

-1

0

1

2

3

-4 -2 0 2 4 6 8 10

Log2 size-class

Log2 size-class

Log 2

(bio

mas

s/∆

wei

ght)

Stan

dariz

ed re

sidu

als

Fig. 5. Integrated normalized biomass size-spectrum and residual

distributions of the macrofauna in the study area.

communities associated to the OMZ present lowdensities and biomass where oxygen levels are extremelylow (e.g. Gallardo, 1963; Rowe, 1971a; Rosenberg et al.,1983; Levin et al., 2000; Levin, 2003). However, higherstanding stocks were observed on the shelf off centralChile in the OMZ, which suggests that these communi-ties could be strongly influenced by oceanographicconditions. In fact, the upper limit of the OMZ issubjected to the influence of oxic waters through short-term downwelling of sub-Antarctic waters (Ahumadaet al., 1983; Gallardo et al., 1995), which might enhancethe biological standing stock and biogeochemicalactivity (Karl and Knauer, 1984; Thompson et al.,1985; Levin et al., 1991, 2000).

It is known that Chl-a and CPE in the sedi-ment are strongly correlated with benthic biomass(e.g. Pfannkuche et al., 2000; Soltwedel et al., 2000).In the study area, pigments (Chl-a and CPE) concen-trations reflect the portion of organic matter input to theseafloor and thus explain the generally elevated standingstock here. Marine benthic communities depend on thesupply of organic matter from the water column above(Graf, 1992). Our results also show significant differ-ences in the standing stock among the study sites and, in

0

200

400

600

800

1000

1200

1400

1600

1800

2000

2200

0,00 0,02 0,04 0,06 0,08 0,10 0,12 0,14

Biomass size-diversity (H*cJ)

Wat

er d

epth

(m)

Iquique (MinOxAntofagasta (PUCK)Concepcion (ETC)Concepcion (PUCK)Chiloe (PUCK)

Fig. 6. Biomass size diversity (Gconfidence interval, 95%) of benthic

macrofauna sampled in the study area.


Table 5

Pearson correlation matrix with the abiotic and biotic variables

Variable Depth Oxygen Mud Chl-a Phaeop CPE TOC C/N

Total density of macrofauna �0.54 �0.28 0.44 0.47 0.44 0.45 0.01 �0.52

Total biomass of macrofauna �0.51 �0.25 0.61 0.63 0.60 0.60 0.03 �0.18

Total biomass of polychaetes �0.56 �0.35 0.53 0.64 0.59 0.60 0.03 �0.31

Total biomass of crustaceans �0.77 �0.76 0.20 0.71 0.70 0.70 0.22 �0.08

NBSS (slope) 0.41 0.57 0.12 �0.28 �0.23 �0.23 �0.20 0.17

NBSS (intercept) �0.49 �0.54 0.51 0.51 0.45 0.45 0.23 �0.31

Total production of macrofauna �0.73 �0.45 0.52 0.64 0.59 0.60 0.01 �0.28

Total production of polychaetes �0.73 �0.48 0.48 0.65 0.60 0.61 0.04 �0.34

Total production of crustaceans �0.86 �0.65 0.16 0.54 0.53 0.53 �0.05 �0.07

Bold letters indicate significant levels ( p! 0.05). The community/population variables and environmental variables were logarithmically

transformed as log10(XC 1).

fact, higher values of primary production have beenobserved off central Chile (0.5–9.6 g Cm�2 d�1) ascompared to northern Chile (0.6–5 g Cm�2 d�1) (Foss-ing et al., 1995; Daneri et al., 2000).

Macrobenthos of the continental shelf associated tothe OMZ, disregarding location, was biologically similarin terms of presenting high macrofauna densities andsimilar species composition. This agrees with findingsreported by Palma et al. (in press) based on a detailedtaxonomical analysis of the communities sampledduring the PUCK Expedition. They reported macro-benthic communities dominated by the polychaetesCossura chilensis, Paraprionospio pinnata, Cirratuluscirratus, Magelona phyllisae and oligochaete sp. A,which contributed 80% to total macroinfauna in theOMZ. This fauna inhabiting the OMZ is adapted to lowoxygen condition (Levin, 2003) by, for example,enlargement of respiratory body surfaces (Lamont andGage, 2000) and capability to conduct anaerobicmetabolism (Gonzalez and Quinones, 2000). In contrast,polychaetes living in the upper and lower slope areassuch as Aphelochaeta monolaris, Aricidea strelzovi,Maldani sarsi, Paramphinome australis, constitutedabout 40% to total macrofauna.

Mean individual weight through their relationshipto productivity emerges as an important parameter anda useful descriptor for estimating the whole-macrofaunacommunity secondary production (Saiz-Salinas andRamos, 1999). In the study area secondary productionwas estimated from P/B ratios derived from the ANNmodel (Brey et al., 1996). P/B is a standardized measureallowing comparisons between species having differentindividual biomass (Cartes et al., 2002). Our P/B valueswere similar to those reported in the study area byCarrasco and Arcos (1980, 1984), providing indepen-dent support for the accuracy of the use of the ANNmodel in these communities. In general, benthic pro-duction showed dependence with water depth. Assum-ing that infauna is composed of approximately 4.3%organic carbon by wet weight (Rowe, 1983), the overallproduction of macrobenthic communities off northern

Chile can be converted from 46.9 g wet wt m�2 y�1 to2.02 g Cm�2 y�1, off central Chile from 158.9 g wetwt m�2 y�1 to 6.8 g Cm�2 y�1, and off Chiloe from19.4 g wet wt m�2 y�1 to 0.83 g Cm�2 y�1. Com-pared with the production estimates of other upwellingareas published by Rowe (1981, 1985) for Peru (2.3 gCm�2 y�1), Baja California (5.2 g Cm�2 y�1), andNorthwest Africa (2.4–3.6 g Cm�2 y�1), the values offnorthern Chile fall within the range of the productionestimates for the same depth range. However, on theshelf off central Chile higher values of production wereobserved. The high values of production reported herefor the whole community, together with those givenfor Carrasco and Arcos (1980, 1984), and values ofstanding-crop of the prokaryontic mat of Thioploca spp.(Gallardo, 1977), confirm that the sublittoral benthosoff central Chile is a highly productive ecosystem.Indeed, the secondary production in terms of carbonequivalents estimated for this ecosystem is higher thanfor other upwelling regions (Rowe, 1971a,b, 1985).Nevertheless, low values of secondary production wereobserved in the OMZ off northern Chile subjected toextremely low oxygen conditions.

It is important to note that one of the most importantlimitations of our calculations is the unknown effect ofhypoxia on benthic P/B ratios. In fact, the physiological,enzymatic, metabolic, reproductive and molecular adap-tations of benthic animals to OMZs are practicallyunknown (Levin, 2003). Furthermore, it is known thatP/B ratios of benthic species under oxic conditions aredependent on environmental factors (Sprung, 1993).Since anaerobic metabolism is less efficient than aerobicmetabolism in terms of energy production per unit (e.g.Burke, 1979), it is highly likely that the P/B ratio of anorganism under hypoxic conditions should be lowerthan that under oxic conditions. In fact, it is known thatP/B is dependent on the rate of instantaneous growth(e.g. Brey, 1998) and there is also empirical evidencethat the growth of both small and large individuals ofthe polychaete Capitella sp. decrease significantly inresponse to reductions in environmental oxygen levels


(Forbes and Lopez, 1990). Therefore our P/B estimatesare likely to be overestimated. Unfortunately, thispotential limitation at our present level of understandingcannot be remedied. Further research in this area isbadly needed.

4.3. Normalized biomass size-spectra

Normalized biomass size-spectra of macrobenthiccommunities off Chile were similar to those also knownfrom other ecosystems (e.g. Drgas et al., 1998; Saiz-Salinas and Ramos, 1999), i.e. normalized biomassversus individual weight followed a linear relation on alog–log scale.

The presence of low oxygen conditions in the HCS offChile obviously has important effects on the sizestructure of the benthic communities living under theseconditions. Schwinghamer (1988) studied unnormalizedbiomass size-spectra of macrobenthic communities inrelation to natural gradients of sediment enrichmentwith organic matter, where body size is more reduced inpolluted sediments. Moreover, Drgas et al. (1998)suggested that BSS of benthic communities living inwell-oxygenated areas are distinctly different from thoseof hypoxic areas. In our study we found small-bodiedmacrobenthos to be more abundant in the communitiesinhabiting the OMZ. This pattern may be explained byphysiological constraints. Small organisms are betterable to satisfy their metabolic demands because theyhave a higher surface area to body volume ratio (Forbesand Lopez, 1990). In fact, Chapelle and Peck (1999)recently proposed maximum body size to be a functionof the availability of dissolved oxygen concentrations.

Residuals distribution of regression analysis showsthe formation of domes (Fig. 4), which might be relatedto trophic organizational/functional groups of organ-isms living in the communities (Dickie et al., 1987;Boudreau et al., 1991; Kerr and Dickie, 2001). Kerr andDickie (2001) have suggested that these types of domesare a consequence of the dependence of P/B ratio onbody size. Quintana et al. (2002) described the presenceof domes in aquatic communities where positive bio-mass residuals are related with high densities of largespecies. In our study area, we also found that large sizeclasses presented positive biomass residuals in thosestations outside the OMZ. In addition we found impor-tant positive biomass residuals in the size class – 1(Fig. 5) that is composed of few polychaetes speciesof small body size such as Aricidea pigmentata andMediomastus brenchiferus. These species have beenpreviously described as highly abundant in habitatsassociated with low oxygen environments and highconcentration of organic matter (Gallardo et al., 1995;Carrasco et al., 1999).

Theoretical models regarding the distribution ofbiomass by size classes have been mostly developed for

pelagic ecosystems (see Kerr and Dickie, 2001 and refer-ence cited therein). This size-spectrum approach allowsa more dynamic interpretation of an ecosystem, becausethe slope of the spectra seems to be related to the energyutilization within the whole community (Rodriguez,1994; Quintana et al., 2002). In our study area, we calcu-lated an integrated normalized biomass size-spectrum(Fig. 5), whose slope (i.e. �0.559, r2Z 0.63) fell withinthe range of those reported for other benthic ecosystems.For instance, Drgas et al. (1998) constructed NBSS forthe Baltic Sea and reported slopes ranging from �0.30 to�0.61. They also calculated an integrated normalizedbiomass size-spectrum with a slope of �0.44. It is knownthat the slope of NBSS can be used as an indicator of theinfluence of environmental conditions on the productiv-ity of aquatic communities (Kerr and Dickie, 2001). Theslope of the integrated normalized biomass size-spectrumfor the whole study area (i.e. including Chiloe,�0.559) ismore negative than that described by Drgas et al. (1998)for the Baltic Sea (�0.44). The low oxygen conditions ofthe subsurface waters of the HCS may be responsible forthis more negative slope.

Low biomass size diversity was found for the benthiccommunities inhabiting the OMZ of the HCS. The eco-logical interpretation of biomass size diversity indices isstill unclear (e.g. Quinones, 1992; Ruiz, 1994) and itsrelationship with community properties such as stabilityand resilience remains an open question. However, forthe pelagic ecosystem it has been argued that the sizestructure might be more sensitive than species diversityto environmental disturbance (Rodrıguez and Mullin,1986). Our results show that the biomass size diversitydecreases with decreasing oxygen concentration, pre-senting less size classes than those found in communitiesliving under normal oxygen conditions. Although noevidence exists yet for a direct connection betweenspecies diversity and biomass size diversity, it is worthmentioning that macro-eukaryotic benthic species di-versity also seems to decline, when environmental con-ditions become harsher (Pearson and Rosenberg, 1978;Levin et al., 2001).

Acknowledgements

We wish to thank all participants of the Thioploca-Chile Expedition (ETC-1999),MinOx Expedition (2000),and PUCK Expedition (2001), who contributed to thestudy’s success. Dr. Lisa Levin provided granulometricdata for the Iquique area, and Dr. Dierk Hebbelnprovided TOC and C/N ratio data from the PUCKExpedition. Thanks to the crew and technicians fromthe Hydrographic and Oceanographic Service of theNavy for help onboard R/V AGOR Vidal Gormaz. Thisresearch was funded by the COPAS center (CONICYT,Chile). The PUCK Expedition was funded by the


German BMBF (No. 03G0156A), ongoing analyses weresupported by the International Bureau of the BMBF(German project number CHL01/010), and the Interna-tional Program of Scientific Cooperation (CONICYT,Chile). E. Quiroga was supported by the FONDECYTGraduate Scholarship No. 402028 (CONICYT) anda MECESUP UCO-0002 Doctorate scholarship. Weacknowledge the comments of two anonymous re-viewers that helped to improved previous versions ofthis work.

References

Ahumada, R., Rudolph, G., Martinez, V., 1983. Circulation and

fertility of waters in Concepcion Bay. Estuarine, Coastal and Shelf

Science 16, 95–105.

Arntz, W., Tarazona, J., Gallardo, V.A., Flores, L., Salzwedel, H.,

1991. Benthos communities in oxygen deficient shelf and slope

areas of the Peruvian and Chilean Pacific coast, and changes caused

by El Nino. In: Tyson, R., Pearson, T. (Eds.), Modern and Ancient

Continental Shelf Anoxia. Geological Society Special Publication,

58, pp. 131–154.

Barnett, P., Watson, J., Connelly, D., 1984. A multiple corer for taking

virtually undisturbed samples from shelf, bathyal and abyssal

sediment. Oceanologica Acta 7, 339–408.

Boudreau, P., Dickie, L., Ker, S., 1991. Body-size spectra of pro-

duction and biomass as system-level indicators of ecological

dynamics. Journal of Theoretical Biology 152, 329–339.

Brey, T., 1998. Growing performance and mortality in aquatic

macrobenthic invertebrates. Advances in Marine Biology 35,

153–243.

Brey, T., Jarre-Teichmann, A., Borlich, O., 1996. Artificial neural

network versus multiple linear regression: predicting P/B ratios

from empirical data. Marine Ecology Progress Series 140, 251–256.

Brey, T., 2001. Population dynamics in benthic invertebrates. A

Virtual Handbook. Version 01.2. http://www.awi-bremerhaven.de/

Benthic/Ecosystem/FoodWeb/Handbook.

Buchanan, J., Kain, J., 1971. Sediment analysis. In: Holme, N.,

McIntyre, A. (Eds.), Methods for Study of Marine Benthos.

IBP Handbook 16. Oxford Blackwell Scientific Publications,

pp. 30–57.

Burke, E., 1979. Aerobic and anaerobic metabolism during activity

and hypoxia in two species of intertidal crabs. Biological Bulletin

156, 157–168.

Carrasco, F., 1997. Sublittoral macrobenthic fauna off Punta Coloso,

Antofagasta, Northern Chile: high persistence of the polychaete

assemblage. Bulletin of Marine Science 60, 443–459.

Carrasco, F., Arcos, D., 1980. Estimacion de la produccion secundaria

de Paraprionospio pinnata (Spionidae; Polychaeta) frente a Bahıa

de Concepcion, Chile. Boletın Instituto Oceanografico Sao Paulo

29, 79–82.

Carrasco, F., Arcos, D., 1984. Life history and production of a cold-

temperate population of the sublittoral amphipod Ampelisca

araucana. Marine Ecology Progress Series 14, 245–252.

Carrasco, F., Gallardo, V.A., Baltazar, M., 1999. The structure of the

benthic macrofauna collected across a transect at the central Chile

shelf and relationships with giant sulfur bacteria Thioploca spp.

mats. Cahiers in Biology Marine 40, 195–202.

Cartes, J., Brey, T., Sorbe, J., Maynou, F., 2002. Comparing

production–biomass ratios of benthos and suprabenthos in macro-

faunal marine crustaceans. Canadian Journal of Fisheries and

Aquatic Science 59, 1616–1625.

Chapelle, G., Peck, L., 1999. Polar gigantism dictated by oxygen

availability. Nature 399, 114–115.

Daneri, G., Dellarossa, V., Quinones, R., Jacob, B., Montero, P.,

Ulloa, O., 2000. Primary production and community respiration in

the Humboldt Current System off Chile and associated oceanic

areas. Marine Ecology Progress Series 197, 41–49.

Dickie, L., Kerr, S., Boudreau, P., 1987. Size-dependent processes

underlying regularities in ecosystem structure. Ecological Mono-

graphy 57, 233–250.

Drgas, A., Radziejewska, T., Warzocha, J., 1998. Biomass size

spectra of near-shore shallow-water benthic communities in

the Gulf of Gdansk (Southern Baltic Sea). Marine Ecology 19,

209–228.

Duplisea, D., 2000. Benthic organism biomass size-spectra in the Baltic

Sea in relation to the sediment environment. Limnology and

Oceanography 45, 558–568.

Eissler, Y., Quinones, R., 1999. Microplanktonic respiration off

Antofagasta (Northern, Chile) during pre-ENSO and ENSO

conditions (1997–98). Journal of Plankton Research 21, 2263–2283.

Folk, R., 1974. Petrology of Sedimentary Rocks. Hemphill, Texas.

Forbes, T.L., Lopez, G., 1990. The effect of food concentration, body

size, and environmental oxygen tension on the growth of the

deposit-feeding polychaete, Capitella species 1. Limnology and


Fossing, H., Gallardo, V.A., Jørgensen, B., Huettel, M., Nielsen, J.,

Candfield, D., Forster, S., Glud, R., Gundersen, J., Kuever, J.,

Ramsing, N., Teske, A., Thamdrup, B., Ulloa, O., 1995.

Concentration and transport of nitrate by mat-forming sulphur

bacterium Thioploca. Nature 374, 713–715.

Gallardo, V.A., 1963. Notas sobre la densidad de la fauna bentonica

sublitoral del norte de Chile. Gayana Zoologica 10, 3–15.

Gallardo, V.A., 1977. Large benthic microbial communities in sulfide

biota under Peru–Chile subsurface countercurrent. Nature 268,

331–332.

Gallardo, V.A., Carrasco, F.D., Roa, R., Canete, J.I., 1995. Ecological

patterns in the benthic macrobiota across the continental shelf off

central Chile. Ophelia 40, 167–188.

Gallardo, V.A., Palma, M., Carrasco, F.D., Gutierrez, D., Levin, L.,

Canete, I., 2004. Macrobenthic zonation caused by the oxygen

minimum zone on the shelf and slope off Central Chile. Deep-Sea

Research II, in press.

Gonzalez-Oreja, J., Saiz-Salinas, J., 1999. Loss of heterotrophic

biomass structure in an extreme estuarine environment. Estuarine,

Coastal and Shelf Science 48, 391–399.

Gonzalez, R., Quinones, R., 2000. Pyruvate oxidoreductases involved

in glycolitic anaerobic metabolisms of polychaetes from the

continental shelf off central-south Chile. Estuarine, Coastal and

Shelf Science 51, 507–519.

Graf, G., 1992. Benthic–pelagic coupling: a benthic view. Oceanogra-

phy and Marine Biology: an Annual Review 30, 149–190.

Gutierrez, D., Gallardo, V.A., Mayor, S., Neira, C., Vasquez, C.,

Sellanes, J., Rivas, M., Soto, A., Baltazar, M., 2000. Bioturbation

potential of macrofauna in sublittoral organic-rich sediments off

central Chile: spatial and temporal variation under ‘‘El Nino’’

1997/98. Marine Ecology Progress Series 202, 81–99.

Hebbeln, D., Marchant, M., Wefer, G., 2000. Seasonal variations of

the particle flux in the Peru–Chile current at 30 �S under normal

and El Nino conditions. Deep-Sea Research II 47, 2101–2128.

Kamykowski, D., Zentara, S., 1990. Hypoxia in the world ocean as

recorded in the historical data set. Deep-Sea Research 37, 1861–

1874.

Karl, D., Knauer, G., 1984. Vertical distribution, transport, and

exchange of carbon in the northeast Pacific ocean: evidence

for multiple zones of biological activity. Deep-Sea Research 31,

221–244.

Kerr, S., Dickie, L., 2001. The Biomass Spectrum. A Predator–Prey

Theory of Aquatic Production. Columbia University Press.

Knap, A., Michaels, R., Dow, R., Johnson, K., Gundersen, J.,

Sorensen, A., Close, F., Howse, M., Hammer, N., Bates, A.,

http://www.awi-bremerhaven.de/Benthic/Ecosystem/FoodWeb/Handbook

http://www.awi-bremerhaven.de/Benthic/Ecosystem/FoodWeb/Handbook


Waterhouse, T., 1993. Bermuda Atlantic Time-series Study

Methods Manual (Version 3). Bermuda biological station for

research, Inc., U.S. JGOFS, 108 pp.

Lamont, P., Gage, J., 2000. Morphological responses of macrobenthic

polychaetes to low oxygen on the Oman continental slope NW

Arabian Sea. Deep-Sea Research II 47, 9–24.

Levin, L., 2003. Oxygen minimum zone benthos: adaptations and

community responses to hypoxia. Oceanography and Marine

Biology: an Annual Review 41, 1–45.

Levin, L., Huggett, C., Wishner, K., 1991. Control of deep-sea benthic

community structure by oxygen and organic-matter gradients in

the eastern Pacific Ocean. Journal of Marine Research 49, 763–800.

Levin, L., Gage, J., Martin, C., Lamont, P., 2000. Macrobenthic

community structure within and beneath the oxygen minimum

zone, NW Arabian Sea. Deep-sea Research II 47, 189–226.

Levin, L., Etter, R., Rex, M., Gooday, A., Smith, C., Pineda, J.,

Stuart, C., Hessler, R., Pawson, D., 2001. Environmental influences

of regional deep-sea species diversity. Annual Review of Ecology

and Systematic 32, 51–93.

Levin, L., Gutierrez, D., Rathburn, A., Neira, C., Sellanes, J., Munoz,

P., Gallardo, V.A., Salamanca, M., 2002. Benthic proceses on the

Peru margin: a transect across the oxygen minimum zone during

the 1997–98 El Nino. Progress in Oceanography 53, 1–27.

Magurran, A., 1988. Ecological Diversity and its Measurement.

Chapman & Hall, London.

Margalef, R., 1957. La teorıa de la informacion en ecologıa. Memorias

Real Academia de Ciencias y Artes, Barcelona 32, 373–449.

McClain, C., Rex, M., 2001. The relationship between dissolved

oxygen concentration and maximum size in deep-sea turrid

gastropods: an application of quantile regression. Marine Biology

139, 681–685.

Menzies, R., George, R., Rowe, G., 1973. Abyssal Environment

and Ecology of the World Oceans. Wiley-Interscience, New York,

467 pp.

Morales, C., Hormazabal, S., Blanco, J., 1999. Interannual variability

in the mesoscale distribution of the depth of the upper boundary of

the oxygen minimum layer off northern Chile (18–24S): Implication

for the pelagic system and biogeochemical cycling. Journal of

Marine Research 57, 909–932.

Neira, C., Sellanes, J., Levin, L., Arntz, W., 2001. Meiofaunal

distributions on the Peru margin: relationship to oxygen and

organic matter availability. Deep-Sea Research 48, 2453–2472.

Palma, M., Quiroga, E., Gallardo, V.A., Arntz, W., Schneider, W.,

Gerdes, D., Hebbeln, D. Macrobenthic animal assemblages of the

continental margin off Chile (22 � to 42 �S). Journal of Marine

Biological Association of the United Kingdom, in press.

Peters, R., 1983. The Ecological Implications of Body Size. University

Press, Cambridge, UK, 329 pp.

Pearson, T., Rosenberg, R., 1978. Macrobenthic succession in

relation to organic enrichment and pollution of the marine

environment. Oceanography and Marine Biology: an Annual

Review 16, 229–311.

Pfannkuche, O., Kahler, A., Sommer, S., 2000. Coupling between

phytodetritus deposition and the small benthic biota in the deep

Arabian Sea analyses of biogenic sediment compounds. Deep-Sea

Research II 47, 2805–2833.

Pielou, E., 1966. Shannon’s formula as a measure of species diversity:

its use and misuse. American Naturalist 100, 463–465.

Platt, T., Denman, K., 1977. Organization in the pelagic ecosystem.

Helgolander WissenschaftlicheMeeresuntersuchungen 30, 575–581.

Platt, T., Denman, K., 1978. The structure of pelagic ecosystems.

Rapports et Proces-Verbaux des Reunions du Conseil International

pour l’Exploration de la Mer 173, 60–65.

Quintana, X., Comin, F., Moreno-Amichi, R., 2002. Biomass-size

spectra in aquatic communities in shallow fluctuating Mediterra-

nean salt marshes (Emporda wetlands, NE Spain). Journal of

Plankton Research 24, 1149–1161.

Quinones, R., 1992. Size-distribution of planktonic biomass and

metabolic activity in the pelagic system. PhD thesis. Dalhousie

University, Halifax, Canada, 225 pp.

Quinones, R., Platt, T., Rodrıguez, J., 2003. Patterns of biomass-size

spectra from oligotrophic waters of the Northwest Atlantic.

Progress in Oceanography 57, 405–427.

Quiroga, E., Soto, R., Rozbaczylo, N., 1999. Los poliquetos

espionidos (Polychaeta: Spionidae) y su importancia en la

estructura de una comunidad: un caso de estudio en Bahıa Iquique,

norte de Chile (20 �11#S; 70 �10#W). Gayana 63, 1–16.

Ramorino, A., Muniz, L., 1970. Estudio cuantitativo general sobre la

fauna del fondo de la Bahıa Mejillones. Revista de Biologıa

Marina, Valparaıso 14, 79–93.

Rex, M., Etter, R., 1998. Bathymetric patterns of body size:

implications for deep-sea biodiversity. Deep-Sea Research II 45,

103–127.

Rex, M., Etter, R., Clain, A., Hill, M., 1999. Bathymetric patters of

body size deep-sea gastropod. Evolution 54, 1298–1301.

Rodriguez, J., 1994. Some comments on the size-based structural

analysis of the pelagic ecosystem. Scientia Marina 58, 1–10.

Rodrıguez, J., Mullin, M., 1986. Diel and interannual variation of

size-distribution of oceanic zooplanktonic biomass. Ecology 67,

215–222.

Rosenberg, R., Arntz, W., Flores, E., Flores, L., Carbajal, C., Finger,

I., Tarazona, J., 1983. Benthos biomass and oxygen deficiency

in the upwelling system off Peru. Journal of Marine Research 41,

263–279.

Rowe, G., 1971a. Benthic biomass in the Pisco, Peru upwelling.

Investigaciones Pesqueras 35, 127–135.

Rowe, G., 1971b. Benthic biomass and surface productivity. In:

Costlow Jr., J.D. (Ed.), Fertility of the Sea, vol. 2. Gordon &

Breach, New York, pp. 441–454.

Rowe, G., 1981. The benthic processes of coastal upwelling eco-

system. In: Richards, F.A. (Ed.), Coastal Upwelling. Coastal and

Estuarine Sciences 1. American Geophysical Union, Washington,

pp. 464–471.

Rowe, G., 1983. Biomass and production of the deep-sea macro-

benthos. In: Rowe, G.T. (Ed.), Deep-Sea Biology. The Sea, vol. 8.

John Wiley & Sons, New York, pp. 97–121.

Rowe, G., 1985. Benthic production and process off Baja California,

Northwest Africa and Peru: a classification of benthic subsystem in

upwelling ecosystems. In: Bas, C., Rubies, P. (Eds.), Simposio

internacional sobre las areas mas importantes del Oeste Africano

(Cabo Blanco y Benguela), vol. 2, Barcelona, Espana, pp. 589–612.

Roy, K., 2002. Bathymetric and body size in marine gastropods:

a shallow water perspective. Marine Ecology Progress Series 237,

143–149.

Ruiz, J., 1994. The measurement of size diversity in the pelagic

ecosystem. Scientia Marina 58, 103–107.

Saiz-Salinas, J., Ramos, A., 1999. Biomass size-spectra of macro-

benthic assemblages along water depth in Antartic. Marine

Ecology Progress Series 178, 221–227.

Schwinghamer, P., 1981. Characteristic size distribution on integral

benthic communities. Canadian Journal of Fisheries and Aquatics

Sciences 38, 1255–1263.

Schwinghamer, P., 1988. Influence of pollution along a natural

gradient and in a mesocosm experiment on biomass-size spectra

of benthic communities. Marine Ecology Progress Series 48,

199–206.

Silva, N., Neshyba, S., 1979. On the southernmost extension of the

Peru–Chile undercurrent. Deep-Sea Research 26, 1387–1393.

Smith, C., Levin, L., Hoover, D., Cremer, M., McMurtry, G., Gage,

J.D., 2000. Bioturbation across the oxygen minimum zone on the

Arabian-Sea slope. Deep-Sea Research 47, 227–257.

Soltwedel, T., Mokievsky, V., Schewe, I., 2000. Benthic activity and

biomass on the Yermak Plateau and in adjacent deep-sea regions

northwest of Svarlbard. Deep-Sea Research 47, 1761–1785.


Sokal, R., Rohlf, F., 1981. Biometry, third ed. WH Freeman and Co,

New York, 859 pp.

Sprules, W., Munawar, M., 1986. Plankton size spectra in relation to

ecosystem productivity, size, and perturbation. Canadian Journal

of Fisheries and Aquatics Sciences 43, 1789–1794.

Sprung, M., 1993. Estimating macrobenthic secondary production

from body weight and biomass: a field test in a non-boreal

intertidal habitat. Marine Ecology Progress Series 100, 103–109.

Stal, L., Van Gamerden, H., Krumbein, W., 1984. The simultaneous

assay of chlorophyll and bacteriochlorophyll in natural microbial

communities. Journal of Microbiological Methods 2, 295–306.

Thiel, H., 1975. The size structure of the deep-sea benthos.

Internationale Revue der Gesamten Hydrobiologie 60, 575–606.

Thiel, H., 1979. Structural aspects of the deep-sea benthos. Ambios

Special Report 6, 25–31.

Thandrup, B., Candfield, D., 1996. Pathways of carbon oxidation in

continental margin sediments off central Chile. Limnology and


Thompson, J., Mullins, H., Newton, C., Vercoutere, T., 1985. Alter-

native biofacies model for dysaerobic communities. Lethaia 18,

167–179.

Williams, P., Jenkinson, N.W., 1982. A transportable microprocessor

controlled precise Winkler titration suitable for field station and

shipboard use. Limnology and Oceanography 27, 576–584.

Warwick, R., 1984. Species size distribution in marine benthic

communities. Oecologia 61, 32–39.

Wishner, K., Levin, L., Gowing, M., Mullineaux, L., 1990. In-

volvement of the oxygen minimum in benthic zonation on a deep

seamount. Nature 346, 57–59.

Wyrtki, K., 1962. The oxygen minima in relation to ocean circulation.

Deep-Sea Research 9, 11–23.

Zar, J., 1984. Biostatistical Analysis, second ed. Prentice-Hall, Engle-

wood Cliffs, NY, 718 pp.

Zuniga, O., Baeza, H., Castro, R., 1983. Analisis de la macrofauna

bentonica del sublitoral de la Bahıa de Mejillones del Sur. Estudios

Oceanologicos 3, 41–62.

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Biomass size-spectra of macrobenthic communities in the oxygen minimum zone off Chile