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Deep-Sea Research II 56 (2009) 1112–1123

Contents lists available at ScienceDirect

Deep-Sea Research II

0967-06

doi:10.1

� Corr

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journal homepage: www.elsevier.com/locate/dsr2

Benthic megafaunal and demersal fish assemblages on the Chileancontinental margin: The influence of the oxygen minimum zone onbathymetric distribution

Eduardo Quiroga a,�, Javier Sellanes b,d, Wolf E. Arntz c, Dieter Gerdes c,Victor A. Gallardo e, Dierk Hebbeln f

a Centro de Investigacion en Ecosistemas de la Patagonia (CIEP), Bilbao 449, Coyhaique, Chileb Universidad Catolica del Norte, Departamento de Biologıa Marina, Larrondo 1281, Coquimbo, Chilec Alfred Wegener Institute for Polar and Marine Research, Columbusstrasse, D-27568 Bremerhaven, Germanyd Departamento de Oceanografıa and Centro de Investigacion Oceanografica en el Pacıfico Sur-Oriental (FONDAP-COPAS),

Universidad de Concepcion, Casilla 160-C, Concepcion, Chilee Laboratorio de bentos, Universidad de Concepcion, Casilla 160-C, Concepcion, Chilef Geowissenschaften, Universitat Bremen, Postfach 330440, D-28334 Bremen, Germany

a r t i c l e i n f o

Article history:

Accepted 12 September 2008Benthic megafaunal and demersal fish assemblages were sampled in three areas off Chile during the

German–Chilean Expedition PUCK (SO-156) onboard the R/V Sonne from March to May 2001, at depths

Available online 5 November 2008

Keywords:

Oxygen minimum zone

Benthic megafauna

Bathyal

Humboldt Current system

Chile

45/$ - see front matter & 2008 Published by

016/j.dsr2.2008.09.010

esponding author. Tel.: 56 67 24 4509; fax: 5

ail address: eduardo.quiroga@ciep.cl (E. Quiro

a b s t r a c t

ranging from 120 to 2201 m. These samples, taken with an Agassiz trawl, are among the deepest ever

taken in Chilean waters. A total of 147 species were recorded, mainly decapod crustaceans (Galatheidae,

Pandalidae, Crangonidae), gastropods (Trochidae, Muricidae, Volutidae), ophiuroids (Asteronychidae,

Gorgonocephalidae, Ophiolepididae, Ophiurinae), asteroids (Pterasteridae, Solasteridae, Goniopectini-

dae), polychaetes (Onuphidae, Aphroditidae, Maldanidae), and demersal fish (Macrouridae, Ipnopidae,

Squalidae). Species richness and rarefaction analyses suggest that the fauna was undersampled. From

the 147 species identified in this study, 36 species (24.5%) occurred only once and another 24 species

occurred only twice (16.3%). Depth and dissolved oxygen levels were found to be the main factors

influencing megafaunal changes along the continental shelf and in bathyal areas, as indicated by

principal component and Pearson’s correlation analyses. Some species appear to be limited to distinct

areas in the upper and lower bathyal zones, whereas other species have a wider range, extending from

the continental shelf to lower bathyal zones. Biogeographic relations exist with the Pacific, South

Atlantic, and Southern Oceans, but the latter seem to be weaker than would be expected considering the

connection by Antarctic intermediate water.

& 2008 Published by Elsevier Ltd.

1. Introduction

Oceanic oxygen minimum zones (OMZs) are ubiquitous andpersistent features on the eastern continental margins of oceanbasins, where dissolved oxygen concentrations decrease to lowlevels (Kamykowski and Zentara, 1990; Levin, 2003; Arntz et al.,2006). These OMZs develop beneath highly productive surfacewaters associated with upwelling, and result from the depletionof oxygen in the water column due to high biological andbiochemical demand (Wyrtki, 1962; Rowe, 1981). OMZs interceptthe continental margin, producing strong gradients of bottomwater dissolved oxygen and organic matter input (Levin et al.,

Elsevier Ltd.

6 67 24 4501.

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2000) and unique biogeochemical processes (Karl and Knauer,1984; Smith et al., 2000). The vertical distribution of benthicpopulations and community structure are greatly influenced bythe presence of OMZs (Menzies et al., 1973; Rosenberg et al., 1983;Arntz et al., 1991; Wishner et al., 1995; Levin, 2003). In general,benthic fauna of the OMZs are dominated by nematodes,oligochaetes, and small-bodied polychaetes, probably associatedwith high food availability and reduced predation pressure (Levinet al., 2002).

The existing literature on megabenthic communities along thecontinental margin off Chile and Peru is restricted mostly to thecontinental shelf and upper slope (e.g., Gallardo, 1963; Brattstromand Johanssen, 1983). In fact, except for the results of the R/VAnton Bruun cruise in the eastern South Pacific (Garth and Haig,1971; Menzies et al., 1973; Tommasi, 1976), the Russian Expedi-tions (Andriashev et al., 1958; Romanova, 1972; Mironov and

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Rudjakov, 1990), and general studies of archibenthal fauna(Frankenberg and Menzies, 1968; Rowe, 1971; Andrade, 1986,1987), there are no detailed ecological studies on bathyalmegabenthic communities. More recently, Sellanes et al. (2004)and Sellanes and Krylova (2005) described diverse chemosymbio-tic assemblages, including various bivalve species (Calyptogena,Lucinoma, Thyasira, Conchocele, Acharax) associated with amethane seepage in the bathyal zone off central Chile (�361S).Notwithstanding, the species composition, diversity, and functionof the megafaunal assemblages in bathyal and abyssal depthsalong the continental margin of the Humboldt Current system(HCS) off Chile and Peru still remain largely unexplored.

Benthic megafaunal assemblages are an important componentin bathyal ecosystems. In fact, the scarce available data suggeststhat benthic megafauna comprise a major fraction of the deepbenthic biomass. Most of the studies on megabenthic commu-nities have focused on the fish fraction and knowledge ofinvertebrates is still limited (e.g., Kallianiotis et al., 2000;Company et al., 2004; Pirtle, 2005; Wicksten and Packard,2005). These studies have identified demersal fish and inverte-brates as one the most important components of biodiversity indeep marine ecosystems; however, their specific habitat require-ments, functional roles, and diversity patterns are not wellunderstood.

Due to logistical constraints, megabenthic community inves-tigations have focused on the continental shelf off northern(Gallardo, 1963) and central Chile (Gallardo et al., 1996). Morerecently, however, quantitative macrobenthic surveys have beenextended onto the continental slope (Palma et al., 2005; Quirogaet al., 2005), including the jointly organized Chilean–GermanExpedition PUCK (SO-156 onboard R/V Sonne) (Hebbeln et al.,2001). One of the main objectives of the PUCK Expedition was todescribe the bathyal benthic communities (i.e. mega, macro,meiofauna) in relation to the extension of the OMZ along thecontinental margin off Chile in specific areas with different localproduction. This paper aims: (1) to characterize the speciescomposition, diversity, community structure, and functionalaspects of the demersal fish and megabenthic fauna; (2) todetermine the effect of the OMZ on the megabenthic community;and (3) to identify the megafaunal assemblages in associationwith the water masses in the eastern South Pacific region off Chile.

2. Methods

2.1. Study area

The regional hydrography of the HCS was recently describedby Schneider et al. (2003). The OMZ core consists of equa-torial subsurface water (ESSW), characterized by high salinity(34.4–34.9 psu) and low dissolved oxygen (o1.0 mL L�1), and istransported southward by the Gunther Current (also known as thePeru–Chile Undercurrent). On the continental margin off Chile,during normal cold (non-El Nino) regimes, the upper border of theESSW mass is located between 50 and 100 m, extending to about350 to 400 m water depth. The low salinity, high dissolved oxygenAntarctic intermediate water (AAIW) flows northward along thecontinental slope between this depth and the Pacific deep water(PDW), which starts at about 1200 m.

2.2. Field sampling

Samples were obtained during Legs 1 and 3 of the R/V Sonne

cruise SO-156 (29 March–14 May 2001). This study (Fig. 1)covered the areas between 221470S and 221510S off Antofagasta,

361020S and 361320S off Concepcion, and 421050S and 421350S offChiloe (Hebbeln et al., 2001). Megafaunal specimens werecollected by means of a modified Agassiz trawl (AGT) with abeam width of 1.5 m and 10 mm mesh size in the codend. A totalof 17 successful hauls were obtained and analyzed. Trawlingdepths of the successful AGT hauls varied from 120 to 2201 mdepth (Table 1), with the latter being one of the deepest ever donein Chilean waters. Collected specimens were preserved on boardin 10% buffered formaldehyde. The time of contact between thegear and the bottom was recorded and these data, together withthe dimension of the mouth opening, allowed a rough calculationof the area swept by each haul in order to estimate relativemegafaunal abundances (Carrothers, 1980).

2.3. Data analysis

A mini-multiple corer with six tubes (inner diameter ¼ 95mm) was used to collect the sediments for chlorophyll (Chl-a) andphaeopigment (Phaeo) analyses (Barnett et al., 1984). Chl-a andPhaeo contents were analyzed photometrically according toLorenzen and Jeffrey (1980). Pigments were extracted from about0.3 g of sediment with 90% acetone in a vortex stirrer, sonicatedfor 10 min, and then centrifuged at 1500� g for 5 min; thisextraction was done twice. The supernatant was used todetermine the Chl-a concentration and then acidified with 0.1 NHCl to estimate Phaeo using a Turner AU-10 fluorometer. The sumof Chl-a and Phaeo is referred to as the chloroplastic pigmentequivalent (CPE) and is used as an indicator of the phytodetritalmaterial input to the sediments (Pfannkuche and Soltwedel,1998). The total organic content of surface sediments total organiccarbon (TOC) was obtained with a Heraeus-CHN-analyzer, byanalyzing 25 mg of homogenized sediments, which were decalci-fied with 6 N HCl and dried on a hot plate at 80 1C. Sediment grainsize analysis was performed using geological sieves and particlesize data were analyzed following Folk (1974). In addition, watercolumn temperature, salinity, and dissolved oxygen were mea-sured at each station using a Seabird CTDO 25 probe mounted on arosette. The output of the oxygen sensor was calibrated usingmeasurements from water samples taken at appropriate depths.Dissolved oxygen was then measured according to the modifiedWinkler method described by Knap et al. (1993), using asemiautomatic version of the photometric end-point detector,Dosimat 665 (Metrohm), and a chart recorder for the titration.

2.4. Statistical analysis

The initial analysis of the megabenthic data included a list ofspecies and numbers of individuals per sample. The megafaunalspecimens were sorted and determined to the lowest possibletaxon. Taxa were assigned to three trophic groups based on theliterature (Menzies et al., 1973; Gage and Tyler, 1991; Sokolova,1997): carnivores, deposit-feeders, and suspension-feeders. Forthe purpose of defining the distribution of megafaunal assem-blages, we designated the following bathymetric zones for thisstudy: sublittoral (i.e. shelf and slope stations from 124 to 365 m),upper bathyal (502–1016 m), and lower bathyal (1380–2201 m)(sensu Hedgpeth, 1957).

To obtain a general view, the megafaunal assemblage struc-tures were analyzed using two diversity indices: Shannon’s H0 (logbase 2) and Pielou’s evenness J0. In addition, the rarefaction (ESn)method, as modified by Hurlbert (1971), was used to compare thediversity of samples of unequal sizes (Magurran, 1988). A principalcomponent analysis (PCA) was used to identify the relationshipsbetween stations with environmental information (James andMcCulloch, 1990). Regression analyses to evaluate relationships

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71067107

7103 7104

22°4

23°4

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PUCK-156Leg 1

7175

7160

7174 7177

7173

7172

71617167

7163

71627166

76° 75° 74° 73°44°

42°

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38°

36°

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N

SouthAmerica

0º

20º

40º

PUCK-156Leg 3

Leg 1

Leg 3

22°9

70°7

7105

7176

Antofagasta

Concepción

Chiloé

75°

Fig. 1. Locations of trawl stations during the PUCK Expedition, 2001.

Table 1Station information and catch data.

Location Leg Station Bathymetric zone Lat. S Long. W Date Haul duration Depth (m) DO % Sand CPE TOC

Antofagasta 1 7104 Sublittoral 22151096 70129039 02.04.01 0650–0717 317–319 0.06 26.22 38.26 4.80

7107 Upper bathyal 22150050 70130093 04.04.01 2144–2240 502–632 0.90 94.47 56.44 n.d.

7103 Upper bathyal 22151099 70132058 02.04.01 1354–1633 864–895 1.28 25.89 31.53 4.99

7106 Lower bathyal 22147098 70132058 04.04.01 1228–1308 1347–1380 1.70 97.97 23.28 3.14

7105 Lower bathyal 22148007 70142029 03.04.01 1732–1842 1649–1900 n.d. n.d. n.d. n.d.

Concepcion 3 7161 Sublittoral 36125052 73123036 23.04.01 2240–2250 120–124 0.45 1.25 85.29 4.28

7160 Sublittoral 36102035 73104040 23.04.01 1225–1240 365–365 0.79 2.24 29.91 2.97

7163 Upper bathyal 36125049 73135072 24.04.01 2221–2236 538–550 2.92 27.48 20.50 2.06

7162 Upper bathyal 36132054 73140005 24.04.01 0804–0819 798–850 2.30 4.31 25.61 2.61

7166 Lower bathyal 36127099 73146047 25.04.01 2015–2029 1294–1424 1.48 3.07 27.16 3.08

7167 Lower bathyal 36127017 73154018 26.04.01 1918–1933 2060–2201 1.82 1.67 31.85 3.04

Chiloe 3 7173 Sublittoral 42105036 74133055 30.04.01 2046–2105 160–185 1.28 58.86 14.03 1.34

7172 Sublittoral 42124061 74147026 30.04.01 1257–1312 286–297 1.52 45.43 14.06 1.56

7176 Upper bathyal 42135035 74148035 02.05.01 2045–2100 480–502 2.79 n.d. n.d. n.d.

7177 Upper bathyal 42134096 74150022 03.05.01 1209–1224 971–1016 2.31 1.78 24.40 3.53

7174 Lower bathyal 42132066 75101010 01.05.01 1548–1605 1445–1776 1.87 1.19 21.20 3.40

7175 Lower bathyal 42127013 75112061 01.05.01 1401–1445 1876–2010 1.93 1.95 17.81 3.12

Samples were taken between April and May 2001.

DO ¼ dissolved oxygen, CPE ¼ chloroplastic pigment equivalents, TOC ¼ total organic carbon.

n.d.: no data.

E. Quiroga et al. / Deep-Sea Research II 56 (2009) 1112–11231114

between water depth and biological diversity measurements werecarried out using the Statistica 6.0 StatSoft, Inc. software for thecombined data set (i.e. Antofagasta, Concepcion, Chiloe).

The correlations between community/population variables (i.e.density, trophic group, community parameters) and environmen-tal variables (i.e. depth, dissolved oxygen, sediment-boundpigments, TOC) were calculated using Pearson’s correlationanalysis. The community/population variables and environmentalvariables were logarithmically transformed as log10(X+1).

3. Results

3.1. Environmental variables

The lowest bottom water dissolved oxygen concentrations(o1 mL L�1) were recorded at stations located on the continentalshelf and upper slope off Antofagasta and Concepcion, i.e. withinthe OMZ associated with ESSW. Oxygen concentrations increasedbelow 632 m off Antofagasta and below 365 m off Concepcion.

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No OMZ was detected off Chiloe, where oxygen concentrationsvaried between 1.3 (shelf stations) and 2.8 mL L�1 (upper bathyalstations) (Table 1).

The sediments sampled off both Antofagasta and Chiloeappeared to be heterogeneous, with higher percentages of sandat the upper and lower bathyal stations. In contrast, sediments offConcepcion were dominated by the mud fractions (Table 1). OffAntofagasta and Concepcion, the highest CPE contents wereobserved in the upper bathyal (56.44mg g�1) and shelf zones(85.30mg g�1), respectively. Off Chiloe, the CPE content rangedfrom 14.03mg g�1 at the shelf station to 24.40mg g�1 around1000 m water depth (Table 1).

The results of the PCA analysis are shown in Fig. 2. The firsttwo PCA axes accounted for 81.1% of the total variance. Theenvironmental variable that most influenced the gradient at thebenthic stations in the study area was water depth. In addition,the sand content was more significant at stations 7172 and 7173(off Chiloe), whereas CPE and Chl-a content exhibited a strongassociation with station 7161 (off Concepcion).

3.2. Faunal composition and vertical distribution

A total of 5785 individuals (mostly adults) were collected,representing 147 species (invertebrates, demersal fishes). In termsof total abundance, decapod crustaceans, gastropods, ophiuroids,asteroids, polychaetes, and demersal fish were the most importantfaunal groups. Although statistical validation of our data was notpossible due to the low number of samples from each bathymetricarea, the general tendency suggests that the most importantgroups at the Antofagasta and Concepcion study sites wereCrustacea, Decapoda, Polychaeta, Mollusca, and demersal fish. Incontrast, Echinodermata was more important than Mollusca andPolychaeta at the Chiloe study site.

Approximately 103 individuals belonging to 23 species(13 families) of demersal fish were collected in the study area(Table 2). All species had been previously reported for the region;9 species belonged to the Macrouridae, 2 to the Squalidae, and 2 tothe Moridae. Trachyrhynchus villegai, Centroscyllium nigrum,Dipturus trachydermus, and Physiculus luminosus were the mostfrequent species in the continental shelf and slope samples(o400 m depth). All Coryphaenoides ariommus, Antimora rostrata,and Coelorynchus chilensis were found at depths between 500 and900 m (upper and lower bathyal sites). Bothrocara alalongum,Bathypterois atricolor, Paraliparis molinai, Macrourus carinatus, and

7104

7103

71067161

71607163

71627166

7167

7173

7172

71777174

7175

DEPTH

DO

SAND

CHL

CPE

TOC

Fig. 2. Principal component analysis (PCA) of environmental variables in the study

area. DO ¼ dissolved oxygen, TOC ¼ total organic carbon, CHL ¼ chlorophyll-a,

CPE ¼ chloroplastic pigment equivalents.

Lampanyctus iselinoides were found at depths 41400 m (lowerbathyal sites).

The decapod crustaceans on the continental shelf and slopewere represented exclusively by Pleuroncodes monodon, Munida

gregaria, and Cancer porteri (Table 2). The decapods Nematocarci-

nus lanceopes, Acanthephyra pelagica, Pandalopsis ampla, Munida

propinqua, Munidopsis trifida, M. opalescens, Pagurus delsolari,Cymonomus menziesi, Eurypodius longirostris, Trachycarcinus hy-

stricosus, and Trachycarcinus corallanus were found at depths4500 m. Metacrangon procax, Pontophylus occidentalis, Stereomas-

tis sculpta, Munidopsis hamata, and Munidopsis rostrata appearedto be frequent at lower bathyal areas (41400 m water depth)(Table 2).

Ophiuroid species were not observed in the continental shelfand upper-slope areas, probably due to the influence of the OMZ.In contrast, many ophiuroid species such as Astrotoma agassizii,Ophiomyxa vivipara, Ophiocantha cosmica, Ophiuroglypha lymani,Gorgonocephalus chilensis, Ophiomusium biporicum, and Ophiomu-

sium lymani were found at depths 4500 m. Ophiocten amitinum,Amphioplus magellanica, Asteronyx loveni, and A. locardi appearedto be restricted to deeper areas (41400 m).

The mollusks Astyris sp. and Cyclocardia velutina were foundexclusively on the continental shelf off Antofagasta and Chiloe,respectively. Zetela alphonsi, Bathybembix macdonaldi, Aeneator

loisae, Fusitriton magellanicus, Trophon vangoethemi, Trophon

condei, Columbarium tomicici, Ptychosyrinx chilensis, Puncturella

sp., Miomelon philippiana, Scaphander cylindrellus, and Leptochiton

americanus were found at depths 4500 m, whereas Solariella nuda

and Yoldiella chilenica appeared at depths 41380 m (Table 2).

3.3. Megafaunal abundances

In general, megafaunal relative abundances showed no cleartrend with increasing water depth (Fig. 3). Along the Antofagastatransect, faunal diversity increased from station 7107 (502–632 mdepth) toward deeper stations. On the same transect, dissolvedoxygen concentrations augmented considerably with depth belowthe OMZ, and ophiuroids, decapod crustaceans (M. hamata, M.

propinqua, M. rostrata, M. trifida), irregular echinoids, and largeforaminifera (Ammodiscus, Cribrostemellus) numerically domi-nated the epibenthos. Megafaunal abundances increased to1380 m depth (702 ind 1000 m�2), mainly dominated by the largetubiculous onuphid polychaete Hyalinoecia sp. (tubes 10–20 cmlength), and then decreased down to 1900 m depth (23 ind1000 m�2). Sites off Concepcion exhibited higher densities at365 and 850 m depth (621 and 742 ind 1000 m�2), whereas thelowest value was observed at the shelf station, inhabited mainlyby P. monodon (16 ind 1000 m�2). The megabenthic abundancesoff Chiloe were greatest at station 7174 (1776 m), where largequantities of the onuphid polychaete Hyalinoecia sp. and scler-actinians were collected (Fig. 3, Table 2). In contrast, station 7176(502 m) revealed the most diverse echinoderm community,including regular echinoids (�50% of the whole catch) andasteroids (Pterasteridae, Solasteridae, Goniopectinidae). Therewere also many gorgonians (Fannyella spinosa, Thouarella sp.). Inaddition, the photographic survey and UW-videos revealed a veryhigh abundance of the majid decapod Libidoclaea granaria,although the AGT failed to support this observation at this station,possibly due to avoidance.

3.4. Community structure

Rarefied sample sizes (ES100) appear to be the best method forunderstanding the low species richness in these samples (Fig. 4).The most evident result is that more samples are required to

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Table 2List of megabenthic species (demersal fish, invertebrates) collected during the PUCK Expedition, 2001.

Taxa Latitudinal distribution Sublittoral stations Upper bathyal stations Lower bathyal stations

Station 7161 7173 7172 7104 7160 7176 7163 7107 7162 7103 7177 7106 7166 7174 7105 7175 7167

Depth (m) 124 185 297 319 365 502 580 632 850 895 1016 1380 1424 1776 1900 2010 2201

Crustacea

Hemisquilla ensiger 36–421 C + + +

Heterocarpus reedi 361 C + ++

Munida gregaria 421 C +

Pleuroncodes monodon 361 C +

Cancer porteri 361 C +

Notiax santarita 361 C + +

Sympagurus haigae 36–421 C + ++ +

Libidoclaea granaria 36–421 C + + + +

Pasiphaea sp 22–361 C + +

Nematocarcinus lanceopes 22–421 C ++ +

Acanthephyra pelagica 22–421 C + +

Merhippolyte sp 22–421 C + +

Pandalopsis ampla 22–361 C + +

Metacrangon sp 22–421 C + +

Munida propinqua 221 C + +

Munidopsis trifida 22–421 C + +

Munidopsis opalescens 22–421 C + +

Munidopsis sp 22–421 C + +

Pagurus delsolari 221 C +

Cymonomus menziesi 22–421 C + +

Eurypodius longirostris 22–421 C + +

Trachycarcinus hystricosus 221 C + +

Trachycarcinus corallanus 421 C +

Haliporoides diomedeae 22–421 C + + +

Campylonotus semistriatus 421 C + ++ + +

Stereomastis suhmi 36–421 C + + + + +

Sclerocrangon atrox 22–421 C + +

Metacrangon procax 221 C +

Nematocarcinus sp 221 C ++

Chorismus sp 221 C +

Pontophylus occidentalis 221 C +

Stereomastis sculpta 221 C + +

Munidopsis hamata 221 C +

Munidopsis rostrata 221 C ++ +

Paralomis sp 22–361 C + +

Lithodidae sp 421 C +

Polychaeta

Kinbergonuphis sp 361 C ++

Onuphis sp 361 C ++

Eunice magellanica 22–361 C ++ +

Hyalinoecia sp 22–421 C +++ +++ +++ +++ +++ + +

Aphrodite longirostris 36–421 C + +

Laetmonice producta 22–421 C ++ + + +

Maldane sarsi 361 D ++ ++ ++

Ninoe chilensis 361 C +

Mollusca

Astyris sp 221 C +++

Cyclocardia velutina 421 S + ++

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Nuculana sp B 361 S + ++ +

Fissidentalium megathyris 36–421 D + + ++ +

Limopsis ruizana 421 S + +

Zetela alphonsi 22–361 D + + +

Bathybembix macdonaldi 22–421 D + ++

Aeneator loisae 22–361 C ++ +

Fusitriton maguellanicus 22–421 C + +

Trophon vangoethemi 22–361 C + +

Trophon condei 22–421 C + +

Columbarium tomicici 221 C +

Ptychosyrinx chilensis 421 C +

Puncturella sp 221 C + ++

Natica sp 361 C + + +

Miomelon philippiana 36–421 C + + ++

Aforia sp 22–421 C + + + + + +

Scaphander cylindrellus 36–421 C + +

Leptochiton americanus 22–421 D + + + +

Fusitaria sp 22–361 D + + +++ ++ ++

Benthoctopus sp A 36–421 C + +

Solariella nuda 221 C +

Solariella sp B 36–421 C + +

Daphnella sp A 36–421 C + +

Yoldiella chilenica 36–421 S ++ ++

Nuculana sp A 221 S ++

Cuspidaria sp 221 S +

Echinodermata

Asteroidea sp G 421 C + +

Echinoidea irregularia sp C 421 D +

Astrotoma agassizii 22–421 D + +

Astroclamys sp 22–421 D + +

Ophiomyxa vivipara 22–421 D + + +

Ophiacantha cosmica 22–421 D + +

Ophiuridae sp A 22–421 D + + ++

Ophiura sp A 221 D +

Ophiura sp B 22–421 D + +

Ophiuroglypha lymani 421 D +

Asteroidea sp E 361 C +

Asteroidea sp H 421 C +

Holothuroidea sp A 221 D +

Crinoidea sp A 421 S +

Gorgonocephalus chilensis 22–421 D + + +

Ophiomusium biporicum 421 D + +

Ophiomusium lymani 22–421 D + + ++ +

Ctenodiscus australis 36–421 C ++ ++ + +

Asteroidea sp A 22–421 C + ++ + + + + +

Asteroidea sp B 22–361 C + + ++

Asteroidea sp C 36–421 C + + + + + +

Asteroidea sp D 36–421 C + +

Phorphosoma sp 36–421 D + + + +

Echinoidea irregularia sp A 22–421 D + + + ++ +

Echinoidea regularia sp A 36–421 D + +

Echinoidea regularia sp A 421 D ++ + +

Echinoidea regularia sp B 421 D ++ + +

Holothuroidea sp B 36–421 D + + + +

Asteronyx loveni 221 D +

Asteronyx locardi 361 D +

Gorgonocephalidae sp 361 D +

Ophiocten amitinum 22–361 D + +++

Ophiura sp C 361 D ++

Amphioplus magellanica 221 D +

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Table 2 (continued )

Taxa Latitudinal distribution Sublittoral stations Upper bathyal stations Lower bathyal stations

Station 7161 7173 7172 7104 7160 7176 7163 7107 7162 7103 7177 7106 7166 7174 7105 7175 7167

Depth (m) 124 185 297 319 365 502 580 632 850 895 1016 1380 1424 1776 1900 2010 2201

Asteroidea sp F 22–361 C + +

Asteroidea sp I 421 C +

Euechinoidea sp 361 D +

Echinoidea irregularia sp B 361 D + +

Echinoidea irregularia sp D 421 D +

Enypniastes sp 361 D +

Sphaerothuria sp 221 D ++

Other invertebrates

Brachipoda sp A 421 S +

Sipunculoidea sp A 421 D +

Thouarella sp 421 S +

Desmospongia sp A 421 S +

Actinaria sp A 22–421 S + + + + +

Actinaria sp B 22–421 S + + +

Echiuroidea sp A 22–421 C + + + +

Pantopoda sp A 22–421 C + + + +

Sipunculoidea sp B 22–421 D ++ + + +

Scleroactinia sp 36–421 S + +++ +++

Fannyella spinosa 36–421 S ++ +

Nemertini sp A 361 C +

Pisces

Trachyrhynchus villegai 221 C +

Centroscyllium nigrum 361 C +

Macrourus sp 361 C +

Dipturus trachydermus 421 C +

Physiculus luminosus 421 C +

Coelorynchus fasciatus 36–421 C + + + +

Aculeola nigra 221 C +

Notacanthus sexspinis 221 C +

Halaelurus canescens 22–361 C + +

Macruroplus potronus 22–361 C + +

Nezumia pudens 22–361 C + +

Eptatretus polytrema 22–361 C + +

Pseudoxenomystax albescens 22–421 C + +

Coryphaenoides subserratus 22–421 C + +

Sagamichthys abei 36–421 C + +

Bothrocara alalongum 22–361 C + +

Bathypterois atricolor 221 C ++

Paraliparis molinai 361 C +

Macrourus carinatus 421 C + +

Lampanyctus iselinoides 421 C +

Coryphaenoides ariommus 22–361 C + + +

Antimora rostrata 22–421 C + + +

Coelorynchus chilensis 36–421 C + + + +

+: occasional (1–10 ind), ++: common (10–100 ind), +++: abundant (100–1000 ind).

Trophic group: C ¼ carnivores, D ¼ deposit-feeders, S ¼ suspension-feeders.

E.

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irog

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/D

eep-Sea

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p>0.05r2 = 0.234n = 17

0

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p>0.05r2 = 0.127n = 17

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p>0.05r2 = 0.072n = 170.0

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p<0.05r2 = 0.487n = 17

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p<0.05r2 = 0.509n = 17

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osit-

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p>0.05r2 = 0.012n = 17

0

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Sus

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ion-

feed

ers

%

500 1000 1500 2000 2500 0Depth (m)

500 1000 1500 2000 2500

0Depth (m)

500 1000 1500 2000 2500 0Depth (m)

500 1000 1500 2000 2500

0Depth (m)

500 1000 1500 2000 2500 0Depth (m)

500 1000 1500 2000 2500

0Depth (m)

500 1000 1500 2000 2500 0Depth (m)

500 1000 1500 2000 2500

Fig. 3. Relationships of water depth to total megafaunal abundances, total species number, diversity (H0), ES100, evenness (J0), percent of carnivores, deposit-feeders, and

suspension-feeders. Significant regression curves and coefficients of determination (po0.05) are shown for analyses based on all available data combined. (m) off

Antofagasta, (�) off Concepcion, (+) off Chiloe.

E. Quiroga et al. / Deep-Sea Research II 56 (2009) 1112–1123 1119

adequately assess diversity in this area. Rarefaction richness forthe Antofagasta samples was lowest at 300 m (ES100 ¼ 2) andincreased with depth to 1300 m (ES100 ¼ 15) (Fig. 4A). Off Concep-cion, rarefaction richness was lowest at 120 m (ES100 ¼ 3),increased with depth to 550 m (ES100 ¼ 21), then declined at850 m (ES100 ¼ 10), and increased with depth to 1424 m(ES100 ¼ 25) (Figs. 3 and 4B). At 1200 m, a collection of 145individuals yielded 25 species, but at 800 m, 514 individualsyielded only 10 species (Fig. 3). Off Chiloe, rarefaction richnesswas lowest at 160 m (ES100 ¼ 5), increased with depth to 500 m(ES100 ¼ 26), then declined at 2000 m (ES100 ¼ 15). Off Antofagas-ta and Concepcion, the lowest diversity values were found at theshelf stations. In general, the number of species tended to increase

with depth to 500 m. In contrast, H0 diversity (Fig. 3) and speciesrichness by rarefaction (Fig. 4C) appeared to be independent ofdepth.

The Pearson’s correlation analysis (pairwise selection)was carried out for all 17 stations in the three study areas,based on six community parameters versus eight environ-mental variables (Table 3). The expected number of species,species abundance, and diversity were positively correlatedwith dissolved oxygen and negatively correlated with thepercent of carnivores. In contrast, the percent of suspension-feeders was negatively correlated with Chl-a, CPE, and TOC.Species richness and density were positively correlated withdepth.

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0

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7104

71037105

7107

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7176

7175

7172

7173

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0Rarefied Samples Size

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0Rarefied Samples Size

250 500 750 1000 1250 1500

Fig. 4. Rarefaction diagram of AGT samples collected as part of the PUCK

Expedition, 2001. Numbers refer to station list. (A) off Antofagasta, (B) off

Concepcion, and (C) off Chiloe.

Table 3Pearson’s correlation matrix between environmental and biotic variables.

No. of species S Abundance N Evenness J0 Exp. spec

Depth 0.75 0.71 �0.18 0.53

Oxygen concentration 0.82 0.42 0.31 0.74Percent of sand �0.25 �0.12 �0.21 �0.24

Chlorophyll-a �0.44 �0.22 �0.29 �0.44

Chloroplastic pigment equivalent �0.40 �0.21 �0.29 �0.42

Total organic carbon �0.11 0.27 �0.66 �0.32

Bold numbers indicate significant levels, po0.05.

E. Quiroga et al. / Deep-Sea Research II 56 (2009) 1112–11231120

4. Discussion

4.1. Influences of the OMZ on megafaunal assemblages

The decrease of megafaunal species diversity, abundance, andbiomass in the ocean with water depth is well documented (e.g.Haedrich et al., 1975, 1980; Smith and Hamilton, 1983; Lampittet al., 1986; Gage and Tyler, 1991). However, some coastalupwelling ecosystems present an exception due to excessivesurface production and the ensuing formation of low oxygenzones on the shelf and upper slope. The major hydrographicfeature of the Humboldt Current region is the presence of apronounced OMZ, which is several hundred meters thick off Peruand northern Chile. In central Chile, the OMZ continues to be asignificant feature, extending in winter from 100 to 300 m waterdepth (Gallardo et al., 1995; Arntz et al., 2006). Early on, Gallardo(1963) sampled the continental shelf and upper slope off northernChile and suggested that the low oxygen concentrations in thewater column have deleterious effects on the benthic fauna. In thepresent study, low abundance values were also observed atcontinental shelf and upper slope sites off northern and centralChile subjected to extremely low oxygen conditions. Megafaunalspecies were almost absent in the OMZ regions where the bottomwater oxygen concentration fell below 0.15 mL L�1, consistent withobservations made in other oxygen deficient settings (see Levin,2003 and reference cited therein). At station 7104 (320 m waterdepth; off Antofagasta), the sediment content was almost entirelycomposed of fish bones with some squid beaks and whale bones(Milessi et al., 2005). However, despite low dissolved oxygenlevels (0.06 mL L�1), many columbellid gastropods (Astyris sp.)were found living among the bones. In fact, Astyris permodesta, aNE Pacific species from the same genus, is common at oxygendeficient settings off California (Bernhard and Reimers, 1991)and Peru (Levin et al., 2002), but also occurs at methane seepsoff California and Oregon, where waters have more oxygen(0.4–0.8 mL L�1) (Levin, 2003). Although the megafauna, particu-larly mollusks, are less tolerant to low oxygen conditions thansmall macro and meiofauna (Levin, 2003; Arntz et al., 2006), it ispossible that these species present enzymatic adaptationsassociated with their anaerobic metabolisms, as described byGonzalez and Quinones (2000) for OMZ polychaetes off centralChile.

Most marine benthic communities depend on a supply oforganic matter from the water column above. In fact, largeinvertebrates appear to be very sensitive to food supply (Sokolova,1997; Ruhl and Smith, 2004). In the study area, macrobenthiccommunities associated with the OMZ present low abundance,biomass, and secondary production values where dissolvedoxygen levels are extremely low (Quiroga et al., 2005). However,higher standing stocks were observed on the continental shelf offcentral Chile, where the upper boundary of the OMZ is subjectedto the influence of oxic waters through short term downwelling ofsub-Antarctic waters (Gallardo et al., 1995; Quiroga et al., 2005)

ies ES100 Diversity H0 Carnivores (%) Deposit-feeders (%) Suspension-feeders (%)

0.25 �0.67 0.72 0.30

0.62 �0.67 0.69 0.60�0.31 0.01 �0.16 0.08

�0.45 0.58 �0.39 �0.73�0.43 0.51 �0.38 �0.74�0.55 0.06 �0.04 �0.70

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that might enhance biological activity and standing stocks (Levin,2003). In the upper or lower boundaries of OMZs, mega andmacrobenthic faunal abundances often exhibit higher values,probably associated with gradients of bottom water dissolvedoxygen concentrations and fresh organic matter input and areduction in predation pressure (Thompson et al., 1985; Levin,2003). Dense megafaunal assemblages of ophiuroids, asteroids,shrimp, crabs, and sponges at OMZ boundaries have beenobserved at Volcano 7 (Wishner et al., 1995), on the Oman margin(Smallwood et al., 1999), off North Carolina (Thompson et al.,1985), and off central California (Smith and Hamilton, 1983);these are associated with high fresh organic matter content(phytodetritus) in the sediments (e.g., Smallwood et al., 1999).

Off central Chile, during 1999, dissolved oxygen concentrationswere lowest at 120 and 206 m depth (o0.13 mL L�1) and highestat 810 m (2.98 mL L�1). At the 364 m station, a dissolved oxygenconcentration of 0.52 mL L�1 was observed (Quiroga et al., 2005).During 2001, low oxygen saturation levels in this area occurredexclusively at 124 m water depth (0.45 mL L�1); at 365 m waterdepth, the critical 0.5 mL L�1 value that characterizes OMZ regionshad already been exceeded. Large quantities (621 ind 1000 m�2)of polychaetes (Hyalinoecia sp., Maldane sarsi) and shrimps(Heterocarpus reedi) were found off central Chile at the 365 mstation (0.79 mL L�1); these were associated with moderate chlor-oplastic pigment concentrations in the sediments (29.91mg g�1). Inaddition, fish abundances of about 120 ind 1000 m�2 were esti-mated. Two species, Centroscyllium nigrum and rat-tails Coelorynchus

fasciatus, were the most important species in the demersal fishassemblages.

In contrast, off northern Chile, no evidence was found of densemegafaunal assemblages at the upper and lower OMZ boundaries.In fact, megafaunal abundance was highest (702 ind 1000 m�2)much below the OMZ, at 1380 m water depth, and was mainlydominated by the onuphid polychaete Hyalinoecia sp. Off Chiloe,megafaunal assemblage abundances exhibited low values(25–83 ind 1000 m�2) on the continental shelf and slope, possiblyinfluenced by the type of substrate, characterized by a high sandcontent according to PCA analysis. Dense megafaunal abundances,which again corresponded to the polychaete Hyalinoecia sp. andscleractinians, were observed at the upper and lower bathyalstations (708 and 1182 ind 1000 m�2, respectively). These dataindicate that low megafaunal assemblage abundances are not onlyproduced by low dissolved oxygen concentrations but also bysubstrate heterogeneity.

4.2. Species assemblages and zonation

Our results suggest that sampling by means of an AGT wasinsufficient to properly characterize the species present in thedifferent areas. Out of the 147 species identified or recorded inthis study, 36 species (24.5%) occurred only once and 24 onlytwice (16.3%). The AGT is only a semi-quantitative gear and, due toits 10-mm mesh in the codend, it does not retain most smaller(e.g., infauna) species. However, this paper is only one out of aseries describing the results of different quantitative and non-quantitative methodological approaches. A comparison of theresults derived from these different methods is underway (Gerdes,unpublished). As of the writing of this manuscript, the taxonomyof numerous species still remained unresolved. In addition, onepolychaete (Hyalinoecia sp.) and three ophiuroids (Ophiura sp.,Amphiophiura sp., Stegophiura sp.) are currently being described asnew. Some species appear to be limited to distinct upper andlower bathyal zones (stenobathic), whereas others are distributedfrom the sublittoral to lower bathyal zones (euribathic). In thisrespect, our results agree with those reported by Andrade (1987)

for central Chile (301–351S) between 250 and 500 m depth. Theauthor identified two main groups: (1) bathyal species (i.e.ophiuroids, asteroids, gastropods) and (2) facultative bathyalspecies with widespread bathymetrical distribution (i.e. decapodcrustaceans, polychaetes, demersal fishes).

A preliminary biogeographical analysis indicates ophiuroidspecies in the study area that also occur in Atlantic waters(Asteronyx loveni, Astrodia tenuispina, Ophiolimna bairdi, Ophiocan-

ta cosmica, Ophiocten amitinium) and sub-Antarctic and Antarcticwaters (Gorgonocephalus chilensis, Astrotoma agassizii). In addition,Ophiomusium lymani, a cosmopolitan species, was also observed(Menzies et al., 1973; Tommasi, 1976; Bernasconi and D’Agostino,1978; Paterson, 1985). In contrast, the decapod crustaceansappeared to be conformed by northern Pacific water species(Guzman and Quiroga, 2005). In fact, the species of the familySergestidae in eastern South Pacific waters consist of two maincomponents: those species shared with the eastern North Pacificand those shared with the western North Pacific (Guzman, 2003).However, among carideans, there are several species living in sub-Antarctic and even Antarctic waters. The asteroids and echinoidsstill require further determination. In summary, our resultsconfirm that bathyal megabenthic fauna in the eastern SouthPacific tends to combine species from the Pacific, the Atlantic, andthe Southern Oceans.

The most common benthopelagic and demersal fish livingon the continental shelf and slope are distributed above the400 m water depth zone (T. villegai, C. nigrum, D. trachydermus,P. luminosus) and contributed 11% of the total fish abundance inthe study area. In contrast, it is important to note that only fourspecies (B. atricolor, H. canescens, C. chilensis, M. carinatus) werethe most common in bathyal areas, representing about 41% of thetotal fish abundances. These species are common in the deep-seaPatagonian tooth-fish (Dissostichus eleginoides) fishery off centraland southern Chile (Oyarzun et al., 2003a) and are characterizedby low fecundity and slow growth (Oyarzun et al., 2003b; Devineet al., 2006). Except for B. atricolor, all these species extend theirareas of distribution to Cape Horn (Sielfeld and Vargas, 1999).Antarctic fish (Notothenioidei), which are still fairly common inthe Magellan region, were not found in the deep-water assem-blages between Antofagasta and Chiloe.

The studies conducted to date seem to indicate that thecomposition of the deep benthic fauna on the continental marginoff Chile and the Antarctic fauna, at least as far as megabenthosand demersal fish are concerned, are basically different despitecertain common trends and even though the two regions areconnected by the influence of AAIW (Palma et al., 2005). Off Chile,many deep epifaunal communities are characterized by their rich,abundant echinoderms, decapods, and colonial cnidarians.Particularly, gorgonians and scleroactinians were more abundantat bathyal stations off Chiloe (i.e. stations 7176 and 7177). Sessileelements, especially sponges, bryozoans, ascidians, and gorgo-nians also prevailed among the megabenthic fauna of the highAntarctic, constituting communities of suspension-feeders with athree-dimensional structure and high diversity and biomass(Gallardo, 1987; Gutt and Starmans, 1998; Arntz et al., 2005).However, suspension-feeder communities comparable to those ofthe high Antarctic have not been found on the three PUCKtransects off Chile. Faunal overlap with the Antarctic Peninsulaalso seemed to be low when compared with that of the Magellanregion (see Arntz and Rios, 1999; Arntz et al., 2005).

The structure and function of bathyal benthic communitiesresult from complex interactions between the biota, sediment,and hydrographic setting. The physical conditions prevailing onthe shelf/slope and in bathyal zones are likely to have the greatesteffect, along with the individual lifestyle requirements ofeach species. In this study, water depth and dissolved oxygen

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concentrations appeared to be the main factors influencing faunalchanges along the continental margin off Chile, distinguished asdifferent depth strata according to their megafaunal compositionby multivariable analysis. In addition, Pearson’s correlationanalysis confirmed the effect of depth and oxygen concentrationson megafaunal assemblages and diversity, suggesting that groupsof stations correspond to ecological bathymetric zones. Asdiscussed earlier, this depressive effect that oxygen has on themegafaunal community’s diversity and abundance at shallowerstations has been clearly documented elsewhere, as has the factthat benthic faunal densities often exhibit a maximum at theupper or lower OMZ boundaries (Levin and Gage, 1998). This peakis often associated with specific oxygen concentrations that mayrepresent a physiological threshold (Levin, 2003). This OMZboundary effect is believed to reflect the interaction betweenthe high availability of organic matter and the absence of anoxygen limitation. In some regions and for selected taxa, thisoccurs within OMZs at extremely low levels of oxygen (0.1–0.2 mLL�1), but the threshold for megafauna seems to be much higher(Thompson et al., 1985; Wishner et al., 1995).

Regression patterns of megafaunal diversity measures wereconsistent with those reported by Levin and Gage (1998) for themacrofauna along a set of depth gradients in the continentalmargins of the North Atlantic, eastern Pacific, and the IndianOcean. As these authors suggested for oxygen-deficient areas,whereas the oxygen concentration basically controls the diversityof benthic assemblages, the sediment organic content correlatesinversely with evenness (Table 3). Moreover, clear differencesfound in species composition along both latitude and depth werethus largely explained by the occurrence of the three previouslymentioned sub-surface water masses in the region. In fact,considering the macrobenthic data obtained during the PUCKExpedition, the station groupings resulting from our data arehighly consistent with those published by Palma et al. (2005). Inconclusion, based on mega and macrobenthic species inventories,our results confirm the influence of ESSW (in turn, associated withoxygen deficient waters, i.e. the OMZ), AAIW, and PDW onbathymetric zonation along the continental margin off Chile.

Acknowledgments

We thank all participants of the R/V Sonne 156 Cruise (PUCKExpedition 2001) who contributed to the success of this study. Theexpedition was funded by the German BMBF (No. 03G0156A) andorganized in the framework of the FONDAP Humboldt Program1997–2000 (CONICYT, Chile). Ongoing cooperation between theAWI and UdeC was funded by the International Bureau of theBMBF (Project No. CHL01/010). This research was funded bythe COPAS center (CONICYT, Chile). The CIEP center (Gobiernoregional de Aysen, BIP, No. 3004258-0) and the Census of MarineLife and affiliated field project COMARGE are thnaked for supportgiven during the writing phase of this work. Taxonomic assistancewas provided by Guillermo Guzman (crustaceans), Dr. MaritzaPalma (polychaetes), Cynthia Lara de Castro Manso (ophiuroids),and Milton Pedraza and Dr. Ciro Oyarzun (fishes). We acknowl-edge the comments of two anonymous reviewers that helped toimprove previous versions of this work.

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