Deep-Sea Research I 68 (2012) 123–135

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Deep-Sea Research I

0967-06

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Factors influencing the distribution of epibenthic megafauna across thePeruvian oxygen minimum zone

Thomas Mosch n, Stefan Sommer, Marcus Dengler, Anna Noffke, Lisa Bohlen, Olaf Pfannkuche,Volker Liebetrau, Klaus Wallmann

Helmholtz-Zentrum fur Ozeanforschung Kiel, GEOMAR, Wischhofstr. 1–3, 24148 Kiel, Germany

a r t i c l e i n f o

Article history:

Received 23 September 2011

Received in revised form

3 April 2012

Accepted 16 April 2012Available online 29 June 2012

Keywords:

Oxygen minimum zone

Epibenthic megafauna

Bacterial mats

Internal tides

Video imaging

Peruvian margin

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

x.doi.org/10.1016/j.dsr.2012.04.014

esponding author. Tel.: þ49 431 600 2267; fa

ail address: tmosch@geomar.de (T. Mosch).

a b s t r a c t

Current de-oxygenation of the oceans is associated with severe habitat loss and distinct changes in the

species composition of bentho-pelagic communities. We investigated the distributions of epibenthic

megafauna across the Peruvian OMZ (111S) at water depths ranging from �80 to 1000 m water depth

using sea floor images. Likely controls of distributions were adressed by combining the abundances of

major groups with geochemical parameters and sea-floor topography. In addition to bottom-water

oxygen levels and organic-carbon availability, particular emphasis is laid on the effects of local

hydrodynamics. Beside the occurrence of microbial mats at the shelf and upper slope, distinct zones of

highly abundant megafauna, dominated by gastropods (900 ind. m�2), ophiuroids (140 ind. m�2), and

pennatulaceans (20 ind. m�2), were observed at the lower boundary of the OMZ. Their distribution

extended from 460 m water depth (O2 levels o 2 mM), where gastropods were abundant, to 680 m (O2

�6 mM) where epifaunal abundances declined sharply. Bottom water O2 represents a major factor that

limits the ability of metazoans to invade deeply into the OMZ where they could have access to labile

organic carbon. However, depending on their feeding mode, the distribution of organisms appeared to

be related to local hydrodynamics caused by the energy dissipation of incipient internal M2 tides

affecting the suspension, transport and deposition of food particles. This was particularly evident in

certain sections of the investigated transect. At these potentially critical sites, energy dissipation of

internal tides is associated with high bottom shear stress and high turbulences and coincides with

elevated turbidity levels in the benthic boundary layer, increased Zr/Al-ratios, low sedimentation rates

as well as a shift in the grain size towards coarser particles. In or near such areas, abundant suspension-

feeding organisms, such as ophiuroids, pennatulaceans, and tunicates were present, whereas deposit-

feeding gastropods were absent. The influence of local hydrodynamic conditions on the distribution of

epibenthic organisms has been neglected in OMZ studies, although it has been considered in other

settings.

& 2012 Elsevier Ltd. All rights reserved.

1. Introduction

Worldwide, oxygen minimum zones (OMZs) are expanding withintegrated oxygen loss rates in the range of 37 mmol m�2 yr�1

(eastern tropical Indian Ocean) and 136 mmol m�2 yr�1 for (easterntropical North Atlantic) (Stramma et al., 2008). These trends areassociated with habitat loss and distinct changes in the speciescomposition of bentho-pelagic communities (Chan et al., 2008; Diazand Rosenberg, 2008). Whereas effects of hypoxia on the distributionof meio- and macrobenthic organisms have been studied at majorOMZs worldwide (Levin, 2003; Gooday et al., 2009) less attention has

ll rights reserved.

x: þ49 431 600 2928.

been paid to epibenthic megafauna and environmental controls ontheir distribution.

As the major OMZs differ in spatial extension as well as in thebottom water (BW) O2 concentration (Helly & Levin, 2004), it isdifficult to generalize distribution patterns of epibenthic mega-fauna. However, successional sequences of microbial and epifau-nal organisms appear to be common to all OMZs. At the upperboundary giant sulfur bacteria belonging to the genera Beggiatoa,Thioploca and Thiomargarita are prominent members of theepibenthos, for instance, off Pakistan (Schmaljohann et al.,2001), off Namibia (Schulz et al., 1999) and on the Peruvian/Chilean continental margin (Gallardo, 1977; Gutierrez et al.,2008). Depending on the BW O2 levels, the core regions of OMZsare mostly devoid of epibenthos (Levin, 2003; Murty et al., 2009).These core regions are characterized by persistently low O2 levels,whereas at the upper and lower boundary of the OMZs bottom

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135124

water O2 levels can be variable on different time scales (Gutierrezet al., 2008; Cowie and Levin, 2009; Sommer et al., 2010). Theboundaries are often densely colonized by epibenthic commu-nities, a phenomenon known as an ‘‘edge effect’’ (Levin, 2003, andreferences therein). It appears that echinoderms, mainly ophiur-oids, dominate such edge communities in all OMZs, with max-imum abundances of up to 140 ind. m�2 off Peru (Levin, 2003;this study). Further epibenthic members are gastropods, penna-tulaceans, asteroids, poriferans, tunicates, crustaceans, holothur-ians, as well as demersal fish (e.g., Levin et al., 1991; Levin, 2003;Gooday et al., 2009; Murty et al., 2009).

Access to abundant food supply within the OMZ has beenrecognized as a major reason for the presence of such edgecommunities. Dependent on their species-specific tolerancetowards oxygen deficiency, organisms seek to invade as deeplyas possible into the OMZ to obtain access to organic carbon that,due to the slow degradation in low-oxic environments, is rela-tively labile (e.g., Wishner et al., 1990). Earlier studies relatedmacrobenthic zonation off Peru and Chile to the vertical structureof different water bodies (Menzies et al., 1973; Levin et al., 2002;Palma et al., 2005). In deep-sea studies the interaction of sea-floortopography with incident internal waves has been considered asan important factor controlling particle deposition and re-suspen-sion and therefore the distribution of epibenthic feeding guilds(Frederiksen et al., 1992; Gage, 2003). Internal waves, which areubiquitous in the global ocean, are dissipated at sloping oceanboundaries generating non-linear bores and turbulences resultingin enhanced bottom shear stress. This causes high levels ofsuspended particles inducing the formation of nepheloid layers(Cacchione and Drake, 1986; Garrett and Gilbert, 1988). Internaltide–topography interactions has been further suggested as aforcing factor governing the large-scale distribution of particulateorganic matter (POM) and fish habitats on the Namibian shelf inthe Benguela upwelling system (Monteiro et al., 2005).

Although sea-floor imaging provides an almost continuousrecord of epibenthos distributions, only a few image-basedstudies described the effects of BW O2 gradients along continentalmargins on the epibenthic megafauna in OMZ environments(Wishner et al., 1990; Smallwood et al., 1999; Gooday et al.,2009; Murty et al., 2009; Sellanes et al., 2010). Moreover, noconsistent small-scale zonation patterns emerge from a compar-ison of different edge communities. Important differences in theabundance of major taxa make it difficult to identify the factorsthat control the structure of epibenthic communities.

Here, we provide detailed information on the zonation pat-terns of epibenthic megafauna on the Peruvian margin derived

Table 1Station list of video casts (OFOS), including start- and endpositons, water depths and n

Station/Gear Date Position start Position end

1W 1S 1W 1S

453OFOS04 08/11/04 77.7995 11.0000 77.8072 11

529OFOS17 08/11/12 77.8247 11.0000 77.8108 11

454OFOS05 08/11/04 78.0173 11.0000 78.0320 11

538OFOS16 08/11/12 78.0392 11.0000 78.0305 11

525OFOS14 08/11/10 78.0417 11.0000 78.0382 11

465OFOS06 08/11/05 78.1575 11.0015 78.1673 10

537OFOS15 08/11/12 78.1795 11.0000 78.1638 11

524OFOS13 08/11/10 78.1915 11.0000 78.1768 11

466OFOS07 08/11/05 78.2480 10.9995 78.2668 10

523OFOS12 08/11/10 78.3333 11.0000 78.3150 11

490OFOS09 08/11/07 78.3330 10.9997 78.3835 10

467OFOS08 08/11/05 78.3838 10.9995 78.4085 10

491OFOS10 08/11/07 78.4058 10.9995 78.4420 10

492OFOS11 08/11/07 78.5200 10.9998 78.5262 11

n No. of still images also includes pictures taken during down- and upcasts of the

from sea floor images that were taken at a high spatial resolutionalong a latitudinal transect at 111S across the OMZ. Image datawere combined with BW O2 levels, geochemical and bathyme-trical data to identify the likely controls on distribution patterns.In addition to BW O2 and the availability of organic carbon (Corg),we hypothesize that local BW hydrodynamics affect small-scaleepibenthic distributions.

2. Methods

2.1. Regional setting

During RV Meteor cruise M77-1/2 (October to December 2008)video imaging, bathymetric, physical and geochemical measure-ments were conducted along a latitudinal depth transect at 111Sacross the Peruvian margin covering a depth range of �80 to1200 m (Table 1; 2; 3). The Peruvian upwelling system is one of theworld’s most productive marine ecosystems (Ryther et al., 1971).High integrated primary productivity of up to 1.3 kg C m�2 yr�1

(Chavez et al., 2011) is sustained by wind driven upwelling, whichtransports cold, oxygen-poor but nutrient-rich water to the well-mixed surface layer. Upwelling is fed by water masses of highsalinity originating from the North, the Equatorial SubsurfaceWater (ESSW), which includes contribution from the Equatorial13 1C Water (Montgomery and Stroup, 1962; Tsuchiya, 1981), theSubtropical Underwater (e.g., O’Connor et al., 2002), and theEastern South Pacific Intermediate Water (ESPIW, Schneideret al., 2003), which is subducted in the southern subtropical Pacificand has low salinity (e.g., Montes et al., 2010). The ESSW istransported southward along the coast of Peru by the Peru ChileUndercurrent (PCU, Brink et al., 1983). Both water masses can befound at depths between 75 to about 500 m and are associatedwith a minimum in dissolved oxygen (Silva et al., 2009). TheAntarctic Intermediate Water (AAIW) is situated below about500 m. This water mass becomes relatively depleted in dissolvedoxygen and nutrients as it moves northwards from the southernpolar front.

Two prominent sediment types characterize the upper con-tinental slope and shelf off Peru (Suess et al., 1987). Between 11and 151S, Corg rich muds (45 wt%) at water depths of 50 and500 m are associated with high bulk sedimentation rates andenhanced preservation and burial. This fine-grained, diatomac-eous, hemipelagic facies forms a thick lens-shaped body extend-ing from the outer shelf to the upper slope at 10.5 to 13.61S(Krissek et al., 1980). In contrast, between 6 and 101S where the

umber of still images taken.

Water depth m No. still imagesn No. still images

Analyzed

Start End

.0000 83 92 102 6

.0000 103 89 73 20

.0000 192 202 0 0

.0000 202 196 70 4

.0000 206 200 44 2

.9997 309 317 0 0

.0000 332 317 114 31

.0000 340 329 93 10

.9998 386 407 182 109

.0000 482 461 135 46

.9995 485 577 304 220

.9998 575 637 168 78

.9998 627 755 216 133

.0000 990 1022 103 21

OFOS.

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135 125

shelf is relatively wide, burial and preservation are reduced owingto continuous re-working of the sediments by cross-shore flowsand alongshore currents, creating a coarse-grained calcareousmud facies (415 wt% CaCO3, Suess et al., 1987).

2.2. Ocean floor observation and image analysis

A total of 14 camera transects was conducted in order torecognise zones with distinct epifauna and sedimentary features(Table 1). A towed camera system (OFOS, Ocean Floor ObservationSystem) equipped with a video- and a still camera (Nikon D70s),two Xenon lights (Oktopus) and a flash light (Benthos) was usedfor sea-floor imaging. This system was towed �1.5 m above thesea floor with an average velocity of about 0.7 knots, resulting inone still image every 15 to 25 m. The position of the OFOS inrelation to the ship was recorded by means of a Posidoniatransponder system. The images were geo-referenced with anaccuracy of better than 10 m using the time label of the stillimages and the ship’s Posidonia navigation data. During a totalobservation time of �23 h, 1158 still images were taken coveringan entire distance of �27 km and an area of �2780 m2. Thedistance of OFOS from the sea floor was controlled by a 20-cm-long, colour-coded ground weight and three laser pointers. Stillimages where faunal identification was impeded by suspendedsediment particles, or by increased distance from the sea bed,were discarded. All other images were post-processed usingAdobe Photoshop CS2. The covered area of each still image wascalculated by means of two laser pointers, which projected tworeference points 50 cm apart from each other on the sea floor.

Epibenthic organisms were identified at least to a highertaxonomic level, and where possible to genus or even specieslevel, and their respective abundances were determined. In thecase of bacterial mats and areas of foraminiferal sands, thenumber of pixels covered by these features were counted andtheir spatial extent was calculated in relation to the total numberof pixels in the entire image. The spatial extent of these facies arepresented in percentages of one square meter. The appearance ofbacterial mats on the sediment surface was classified as patches,threads or a mixture of both. The determination of tunicateabundance involves uncertainties as they were often obscuredby other organisms. The presence of gastropods, often visible onlyas whitish objects in the images, was verified from sedimentsamples.

Table 2Station list of CTD water sampling rosette casts and physical parameters at the bottom

Station/Gear Date Position

1W 1S

430CTD12 08/11/02 78.1413 10.9998

476CTD24 08/11/06 78.2533 11.0017

545CTD35 08/11/12 78.3410 10.9997

428CTD11 08/11/02 78.3418 11.0018

515CTD33 08/11/09 78.3923 10.9968

444CTD20 08/11/03 78.4108 11.0000

443CTD19 08/11/03 78.4258 11.0000

020CTD60 08/11/30 78.4322 10.9960

442CTD18 08/11/03 78.4382 11.0000

441CTD17 08/11/03 78.4573 11.0000

424CTD09 08/11/02 78.5003 11.0007

501CTD32 08/11/08 78.5167 11.0000

547CTD37 08/11/12 78.5210 10.9997

438CTD16 08/11/03 78.5837 11.0115

463CTD22 08/11/04 78.7477 11.0002

2.3. Water column oxygen, temperature, salinity and turbidity

Turbidity was measured at a sampling rate of 30 seconds asFTU (Formazine Turbidity Units) using a Seapoint Auto rangingsensor (accuracy o2%) that was mounted on the OFOS. For thephysical characterization of the water column conductivity-tem-perature-depth/oxygen (CTD/O2) profiles were sampled (Table 2)using a SBE 911 plus CTD-system manufactured by SeabirdElectronics Inc. of Bellevue, Washington, USA. The CTD/O2 systemwas attached to a rosette holding 24 Niskin bottles that were usedfor water sampling.

2.4. Multibeam bathymetric survey, determination of critical sea

floor areas

Multibeam surveys were conducted using the shipboard echo-sounder system EM120 (12 kHz, 191 beams). Post-processing ofthe multibeam data was performed using MB System 5.1.1(Caress and Chayes, 2001). Multibeam bathymetric data are usedin combination with CTD profiles along the continental slope toinvestigate energy conversion from barotropic and low-modebaroclinic tides to high-mode baroclinic tides of short verticalwave length. The magnitude of this conversion is controlled bythe slope of topography (a, derived from the Multibeam data at aspatial resolution of �30 m) and the slope of propagation of thelarge-scale low-mode baroclinic tide b, which is defined asc¼((s2

� f2)/(N2�s2))1/2

¼tan(b), where s is the frequency ofthe internal tide, f is Coriolis parameter and N is buoyancyfrequency. b was calculated for the dominant M2 (semidiurnal)tidal frequency. To evaluate the slope of internal wave propaga-tion, buoyancy frequency squared N2

¼(g/r0)n(dr/dz)�g2/c2

(where g is the earth gravity acceleration, r0 is the potentialdensity, c is the speed of sound, and dr/dz is the vertical oceanicdensity gradient) was determined from the CTD data using theadiabatic leveling method (Fofonoff, 1985). For each CTD profilean average value for N was calculated for the depth rangebetween 100 and 200 m above the sea floor to exclude valuesfrom the bottom boundary layer. An algorithm tool provided byMatthias Tomczak (Flinders University, Australia) at http://gaea.es.flinders.edu.au/�mattom/Utilities/bvf.html was used forthe calculation.

Topographic slopes are classified as transmissive (subcritical,aob), critical (aEb), and reflective (supercritical, a4b) (e.g.,Holloway, 1985). Upon reflection, internal waves preserve their

water (BW).

Water depth

m

BW O2

mM

BW temp.

1C

BW sal.

299 1.01 12.03 34.88

399 1.86 8.27 34.64

475 1.75 8.39 34.65

508 1.78 8.09 34.63

598 4.05 7.19 34.59

656 9.43 6.27 34.57

705 11.73 6.06 34.56

720 6.63 6.66 34.58

753 16.78 5.71 34.56

809 24.20 5.32 34.55

944 38.71 4.75 34.55

1001 40.34 4.69 34.55

1017 40.09 4.72 34.55

1282 63.74 3.56 34.58

2059 93.23 2.26 34.65

Table 3Station list of sediment sampling sites (MUC and BIGO), including water depth (W. d.), geochemical and sedimentological characteristics from the sediment surface (0–

1 cm sediment depth).

Station/Gear Date Position W. d. Corg Opal CaCO3 Sed. rate Sand Silt Clay Molar ratios

1W 1S

M wt% wt% wt% cm kyr�1 wt% wt% wt%

Zr/Al C/N

543MUC52 08/11/12 77.7900 10.9998 85 3.50 16.56 2.06 70 15.30 78.20 6.50 17.06 8.80

470MUC29 08/11/05 77.9433 11.0003 145 7.61 18.80 5.77 n.d. 15.50 78.70 5.80 18.55 8.72

449MUC19 08/11/03 78.1662 11.0002 319 10.65 12.40 19.49 50 20.00 76.70 3.30 20.62 8.83

016BIGOT6 08/11/29 78.0985 11.0002 259 13.54 15.18 1.59 n.d. n.d. n.d. n.d. 18.29 10.43

481MUC33 08/11/06 78.2365 11.0000 376 10.86 7.80 21.89 n.d. 20.40 76.50 3.10 38.75 8.91

519MUC43 08/11/10 78.2715 11.0002 410 8.50 4.59 31.72 n.d. 27.30 70.30 2.40 41.20 9.21

455MUC21 08/11/04 78.3205 11.0000 466 4.50 1.78 36.51 n.d. 39.10 58.30 2.60 49.13 9.41

516MUC40 08/11/09 78.3333 11.0000 512 6.07 0.74 33.43 20 29.30 65.00 5.80 57.53 9.79

487MUC39 08/11/06 78.3862 11.0003 579 6.48 2.18 29.97 26 34.50 63.30 2.20 47.39 9.29

459MUC25 08/11/04 78.4267 11.0005 697 6.72 2.12 31.08 81 24.10 71.10 4.80 35.29 9.98

025BIGO7 08/12/01 78.4350 10.9958 716 8.08 30.73 n.d. n.d. n.d. n.d. n.d. 11.36

445MUC15 08/11/03 78.5003 11.0000 928 5.15 1.78 6.84 n.d. 38.60 58.40 3.00 34.45 9.41

013BIGO6 08/11/29 78.5175 11.0002 978 4.09 16.51 n.d. n.d. n.d. n.d. n.d. 9.88

549MUC53 08/11/13 78.5212 11.9968 1005 4.00 1.97 17.90 45 38.70 58.90 2.40 36.71 10.92

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135126

angle to the horizontal rather than to the reflecting surface(Phillips, 1977), so that reflection from slopes near the criticalangle leads to reflected waves with higher wave numbers andgreater shear (e.g., Eriksen, 1982). The energy of these waves willbe amplified and its progress slowed, causing it to break and toproduce turbulence (Garrett and Gilbert, 1988). In addition, whenthe horizontal velocity of the wave approaches the wave phasespeed, non-linear processes need to be considered. Transforma-tion of the wave into an internal bore, a series of distinct highfrequency waves or wave trains having smaller wavelength, mayoccur (e.g., Schafstall et al., 2010).

2.5. Sediment sampling

A TV-guided multiple corer (MUC) was deployed to retrievesurface sediment samples (Table 3). After retrieval of the MUCone core tube was immediately transferred to the cool-room,which was maintained close to in situ temperature (4–8 1C). Aftercareful removal of the bottom water by siphoning, each sedimentcore was extruded and sliced at 1 cm intervals for the top 5 cmand into 2 cm intervals for sediment deeper than 5 cm. After porewater extraction, the squeeze cakes were collected for furtheranalysis at the shore-based laboratory. In addition, �5 ml of wetsediment were collected and stored at about 4–8 1C for thedetermination of the water content and the porosity. Furthersurface sediments were obtained from the flux chambers of thebiogeochemical observatories (BIGO and BIGO-T). The functionalprinciple of these chamber landers has been described by Sommeret al. (2009). During this study only results from the uppermostsediment were used.

2.6. Particulate organic carbon, carbonate and C/N-ratio in surface

sediments

The squeeze cakes were freeze-dried and ground in an agatemortar. Total content of C and N was determined by combustionof the surface sediment samples using a Carlo–Erba elementanalyzer (NA 1500). An additional set of sediment samples wasused for the determination of the Corg content. Prior to the Cmeasurements these sediment samples were acidified with HCl toremove carbonates. The difference between total C and Corg

content represented the carbonate content. Sediment and soilstandards with certified concentrations of C and N were analysedduring each run (marine sediment MAG-1, United States geolo-gical Survey; soil standard 1, HEKAtech GmbH). For the detailed

description of the applied methods see http://www.ifm-geo-mar.de/index.php?id¼mg_cns-bestimmung&L¼1.

2.7. Biogenic silica (BSi)

The biogenic opal content of the freeze-dried and groundsurface sediments was measured with an automated wet-leach-ing method (Muller and Schneider, 1993). The precision of thismethod is better than 2% for opal-rich samples and 4–10% forsamples with an opal content less than 10 wt%. The biogenic opalvalues are given as SiO2 concentrations in wt% not considering thewater content of this compound.

2.8. Aluminium (Al) and zirconium (Zr)

The freeze-dried and ground surface samples were analysedfor these elements by XRF using a Philips PW 1480 sequentialX-ray spectrometer. The elements were determined on fusedglass disks, prepared in a platinum crucible by mixing of600 mg of each sample with 3600 mg of lithiumtetraborate(Li2B4O7, Spectroflux 100). Further information is available athttp://www.ifg.uni-kiel.de/189þM52087573ab0.html.

2.9. Grain size, water content, porosity

For grain-size analysis, sediments from the surface (0–1 cm)were treated with HCl (10%) to dissolve the carbonates and withH2O2 to remove the organic content. Addition of Na4P2O7

nH2O(0.1 M) inhibited subsequent re-agglomeration of single particles.Grain-size distribution was determined by laser diffraction tech-nique using the Mastersizer 2000 system (Malvern Instruments).Grain-size sampling spanned the range from 0.02 to 2000 mm; theprecision was 1%. Statistical data processing was conducted usingthe Gradistat software tool (Blott and Pye, 2001). Water contentand porosity were determined by the weight difference beforeand after freeze-drying of wet sediment samples. Values wereconverted into a volume ratio (volume of pore water/volume ofbulk sediment) assuming a dry sediment density of 2 g cm�3 anda seawater density of 1.024 g cm�3.

2.10. 210Pb sedimentation rates

Sedimentation rates were determined at 6 sites (cf. Table 3).Up to 10 g freeze-dried and ground sediment from the differentdepth intervals was embedded into a 2-phase epoxy resin (WestSystem Inc.). Prior to the analysis by non-destructive counting of

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135 127

gamma-ray activity, the embedded sediment was allowed toequilibrate for at least three weeks to ensure steady statebetween 226Ra and 214Bi. A low-background coaxial Ge(Li) detec-tor was used to measure total 210Pb via its gamma peak at46.5 keV and 226Ra via the granddaughter 214Pb at 352 keV. The210Pbtot values were corrected for the natural decay of 226Ra toobtain the unsupported (excess) fraction (210Pbxs) induced by theatmospheric input which is used for the determination of sedi-mentation rates (Schelske et al., 1994). Assuming steady stateconditions, sedimentation rates were calculated using the excessactivity of 210Pb, depth-dependent porosity and bioturbation(Meysman et al., 2005).

Fig. 2. Average slope angle along the 111S depth transect. Averages and standard

deviations (indicated by dark grey area, nE30) were calculated for 1000 m

horizontal distance intervals along the transect. Slope angles were determined

at a horizontal resolution of 30 m. The light grey area indicates bottom water O2 in

the range of 2 to 20 mM, the dark grey area represents the core of the OMZ with

O2o2 mM.

Fig. 3. Average ratio between the slope angle a and the propagation angle of the

semidiurnal internal tide (M2), b. Only one value for b for each CTD cast was

determined. Averages and error bars were calculated from 25 m depth intervals.

3. Results

3.1. Water column oxygen and turbidity

Lowest O2 levels (o2 mM) extended from about 50 m down to�500 m water depth (Fig. 6, Table 2). The upper oxycline wascharacterized by a steep gradient whereas the lower OMZboundary displayed a rather gradual increase of BW O2 to�40 mM at 1000 m water depth. Highest turbidity values (up to4 FTU), representing high particle load, were measured in thebottom boundary layer within the OMZ, especially around 200 mwater depth but also further downslope at �740 m (Fig. 1).Higher turbidity was generally associated with changes in topo-graphy except at �340 m. At these points, nepheloid layers canbe traced up to 15 km offshore, particularly at �200, 320 and740 m, but also, although less distinctly, at 510, 580 and 620 mwater depth. In the photic zone, as well as throughout the entirewater column at the shallow sites (90–100 m), increased turbiditywas determined during the down- and upcasts of the OFOS.

3.2. Bathymetry and critical slope

The slope of the sea floor changed distinctly with increasing waterdepth and distance from the coast (Fig. 2). The shelf area down toabout 200 m was rather flat and displayed an average slope angle of0.251. Beyond 200 m, the slope angle changed to 0.61 down to 500 m.Between 500 and 600 m water depth the slope angle was 11 andfurther increased to 21 at about 1000 m. Remarkable, rather abruptchanges in the slope angle were observed at 500 m, 600 m and 720 mwater depth. The topography between 100 and 500 m water depth

Fig. 1. Contour plot of turbidity (FTU) across the latitudinal depth section at 111S,

reconstructed from 14 OFOS casts (grey crosses). Data were interpolated using the

inverse distance to a power gridding method.

For each depth interval changes in the average slope angle that was determined

with a horizontal resolution of 30 m and respective standard deviation was

calculated and related to b determined for the appropriate water depth. The

number of slope changes (n) determined for each depth interval was dependent on

the overall steepness considered in the respective depth interval. Critical condi-

tions at a/bE1 are indicated by a black dashed line. Grey area indicates water

depths where the slope potentially becomes critical.

was smooth, as indicated by a low standard deviation of the slopeangles in this area (Fig. 2), which is in contrast to the roughtopography at greater water depths.

The investigated transect at 111S could potentially become criticalor near critical at several points; around 500 m, a larger regionbetween 610 and 680 m, and between 720 and 740 m water depth(Fig. 3). This is mainly due to the fact that the slope angle a increasesat water depths greater than 500 m, but stratification remainselevated (NE3�10�3 s�1) down to �740 m water depth (whichmeans a low propagation angle b of internal waves) and decreasesrapidly down-slope. However, in common with continental marginsworldwide (Cacchione and Drake, 1986), much of the sea-floortopography was classified as subcritical, indicating that the energyof incident internal M2 tides was transferred up-slope.

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135128

3.3. Geochemistry of surface sediments

The latitudinal distribution of Corg showed a pronouncedmaximum of 13.5 wt% within the core of the OMZ at 259 m anda second maximum of 8.1 wt% at 716 m water depth (Fig. 4).Except at the shallow shelf site (85 m), the Corg contents in allsamples was greater than 44 wt%. The molar C/N-ratio variedbetween 8.7 and 11.4 with higher values indicating the presenceof less labile organic carbon. Except for the highest C/N-ratios at259 m (10.4) and 716 m (11.4), there was a trend of increased ofrefractory organic matter with increasing water depth.

Biogenic opal in the surface sediments showed a distinctmaximum on the shelf (18.8 wt%) and decreased steadily towardsthe lower edge of the OMZ (0.7 wt%). At water depths greater than500 m biogenic opal remained almost constant at �2 wt%. Exceptthe shelf stations, its distribution was similar to that of Corg,indicating that below 200 m water depth hemi-pelagic diatomac-eous organic carbon represent a major carbon source, whereas theshelf station receives terrestrial Corg input. In comparison tobiogenic opal, the carbonate content exhibited an almost inversedepth distribution with high values in the range of 30 to 37 wt%below 350 m water depth, indicating a strong transition betweenthe input of diatomaceous and carbonaceous material.

The Zr/Al-ratio can be used as an indicator for particle depositionand erosion. In comparison to Zr, Al is more mobile under elevatedBW current velocities, where it becomes suspended and transportedto locations with lower bottom shear stress (Ganeshram et al., 1999;Boning et al., 2004). Inside the OMZ, low Zr/Al-ratios indicate a ratherdepositional regime whereas erosional conditions are indicated forthe depth range between �400 and 600 m and to a lesser extentbelow 600 m.

The shelf and upper slope sediments are mainly composed ofsilts with �80 wt% (Fig. 4). However, below 400 m the siltfraction decreased, whereas the proportion of sand increased to

Fig. 4. Geochemistry of surface sediments along the latitudinal transect at 111S.

The light grey area indicates bottom water O2 in the range of 2 to 20 mM, the dark

grey area represents the core of the OMZ with O2o2 mM.

about 30–40 wt%, indicating a more erosional BW current regime.Minimum sedimentation rates of �20 cm kyr�1 were measuredat the 500 and 600 m sites, confirming the presence of anerosional regime in this area.

3.4. Sea floor observation

The still images revealed distinct zones characterized bydifferent epifaunal megafauna and the occurrence of filamentous,mat-forming sulfur bacteria. Patches of microbial mats, presum-ably of the genera Thioploca and Beggiatoa (Fig. 5a), were observedin water depths of 80 to 400 m. The spatial extent of these matswas highest on the shelf, but did not exceed 10% coverage.Microbial patches were visible at 200 m, but the images werestrongly obscured by a high particle load in the BW impeding thedetermination of their spatial extent. At water depths of 300 to400 m bacterial mats displayed a rather thread-like appearance(Fig. 5b). Sediment samples that were retrieved during MUC andBIGO deployments in water depths of 85, 259, and 319 mconfirmed the widespread occurrence of these microbial mats.Spionid polychaetes were observed in association with microbialmats (Fig. 5b, arrows; c). This was confirmed by sedimentsrecovered during the deployment of BIGO 5 (85 m). They werealso resolved in still images obtained from deeper regions (�320to 340 m), where they form aggregations up to 6 cm in size. Thesepolychaetes were also associated with black sediment patchesand long extended whitish strands of microbial mats. The spionidpolychaete depicted in Fig. 5c belongs either to the genusParaprionospio or to Prionospio. The difference between thesetwo genera cannot be resolved from the photographs. However,since there is abundant Paraprionospio off Chile (Quiroga et al.,2007), it is likely that this species belongs to this genus.

Distinct zones characterized by different megafaunal metazo-ans occurred across the lower boundary of the OMZ. Gastropodsbelonging to the species Astyris permodesta (Dall, 1890) (syn. Alia

permodesta) (Fig. 5d; e) densely colonized the area between 460and 480 m, with maximum abundances of up to 900 ind. m�2.Except for fish, these organisms penetrated furthest into the OMZ.Bentho-pelagic fish of the family Macrouridae were encounteredbetween 390 and 740 m water depth. At water depths between485 and 520 m the gastropods were superseded by tunicates(Fig. 5f) and poriferans (Fig. 5h). There was almost no spatialoverlap between these two zones. Arborescent foraminifera of thegenus Pelosina were identified between 475 and 560 m (Fig. 5f; g).These protozoans were particularly prominent between 485 and530 m, where they formed dense clusters up to 25 cm in dia-meter, which were closely associated with poriferans or tunicates.At �560 m water depth pennatulaceans appeared, with a max-imum density of 20 ind. m�2 (Fig. 5i). These organisms displayedan extremely well-defined distribution pattern that was closelyassociated with the presence of tunicate larvae floating in thebottom water.

At greater depths, between 580 and 680 m, echinoderm com-munities dominated by ophiuroids were observed (Fig. 5j; k).These organisms displayed a skewed distribution with theirabundance maximum (140 ind. m�2) shifted towards theirshallower distribution limit at 620 m (Fig. 6). However, asteroidsand holothurians were also present in high abundances (6 and 16ind. m�2, respectively), with their maxima being located slightlydeeper at �650 and 670 m water depth, respectively. Colony-forming tunicates associated with hard ground, single poriferans,and a few other organisms including gorgonians, octopods(Fig. 5l) and anemones, were also present in this depth. Crusta-ceans, predominantly galatheid crabs of the genus Munidopsis,were observed in water depths from 640 to 740 m (Fig. 5m),where they create large holes with diameters of up to �2 cm in

Fig. 5. Sea floor observation. (a), patches of bacterial mats and ripple structures (OFOS 17, 96 m); (b), long whitish strands of bacterial mats and polychaetes (white arrows,

OFOS 15, 322 m); (c), Spinoid polychaete in bacterial mat sediments (benthic chamber BIGO 5, 85 m); (d), gastropods (OFOS 12, 461 m); (e), detail of a gastropod (Astyris

permodesta) (MUC 22, 465 m); (f), tunicates, cluster of arborescent foraminifera and macrouridae (OFOS 09, 507 m); (g), detailed side view of arborescent foraminifera

(Pelosina sp.) (MUC40, 512 m); (h), yellow sponge, ophiuroids and other megabenthic epifauna (OFOS 08, 597 m); (i), pennatulaceans (OFOS 09, 571 m); (j), echinoderm

community (ophiuroids, holothuroids, asteroids, OFOS 10, 643 m); (k), dense ophiuroid assemblage, hardground (OFOS 10, 672 m); (l), hardground, populated by diverse

megafauna (OFOS 10, 729 m); (m), crustacean (white arrow), leaving feeding traces on dark greenish detritus around its burrows (OFOS 10, 688 m); (n), foraminiferal sand

(MUC 22 465 m). The length of colored ground weight is 20 cm, suspended 1.5 m below the Ocean Floor Observation System (OFOS). White scale bars: a, b, d, f, h, i, j, k, l,

m: 50 cm; c, e, g, n: 0.5 cm.

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135 129

the sea floor. It appears that these crustaceans undertake feedingexcursions, grazing on the dark, olive-green detritus and therebyexposing bright spots of foraminiferal sands.

At water depths between 740 and 750 m, sea–floor observa-tions were impeded by high particle load in the BW. Althoughforaminiferal sands (Fig. 5m; n) were present between 400 and700 m, they were recorded mainly at 460 and 620 m. Theseregions were dominated by gastropods and echinoderms, respec-tively. No images were obtained from 755 to 990 m. At waterdepths below about 1000 m, there were no conspicuous sea-floorfeatures. Small ophiuroids and pennatulaceans were sporadically

observed and the sediment surface was characterized by holes ofdifferent sizes and shapes.

4. Discussion

4.1. Mat-forming bacteria

A clear spatial sequence of epibenthic megafaunal taxa wasevident along the investigated depth transect across the PeruvianOMZ. The shelf and upper slope down to 400 m, water depth

Fig. 6. Epibenthic species distribution along 111S. Spatial extent of bacterial mats and foraminiferal sands shown as proportional coverage per m�2. The abundances of all

other groups is given as no. of individuals m�2. Depth ranges were images were taken are shaded in grey. Oxygen (mM), temperature (1C) and salinity data were measured

during CTD cast 16 at 1282 m water depth.

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135130

characterized by BW O2 concentrations o2 mM, were colonized bymat-forming sulfur bacteria, presumably belonging to the generaThioploca and Beggiatoa, which have been observed also during earlierstudies at the Peru–Chile margin (e.g., Gallardo, 1977; Levin, 2003). Insitu nitrogen flux measurements (Sommer et al., unpubl.), conductedduring the same cruise, in combination with a modeling study(Bohlen et al., 2011), suggested that these bacteria profoundly affectthe benthic nitrogen cycle by performing DNRA (dissimilatory nitratereduction to ammonium), thereby releasing large amounts of ammo-nium into the BW. By limiting the removal of the fixed nitrogen thatis common in margin sediments, these bacteria provide a potentialpositive feedback to surface primary production.

Mat-forming sulfur bacteria are dependent on elevated BWlevels of nitrate (and possibly nitrite) and high primary produc-tion that sustains high sulfide production from sulfate reduction,in addition to periodic anoxia (Jørgensen and Nelson, 2004, andreferences therein). The shelf at 111S likely is subjected toperiodic BW oxygenation events similar to those that wereobserved at a 94-m-deep station at 121S off Callao, whereintermittent oxygenation events, caused by the passage of coastaltrapped waves (CTWs), apparently favor the colonization ofThioploca (Gutierrez et al., 2008). Off Callao, vertical fluctuationsof the upper boundary of the OMZ have been observed between10 and 90 m water depth over a period of 13 years (1992–2005).During strong positive El Nino Southern Oscillation (ENSO)

conditions, CTWs occur more frequently (Gutierrez et al., 2008)and oxygenation events are likely to reach water depths down to300 m (Levin et al., 2002). In conjunction with a sharp transitionbetween low nitrate but high nitrite levels at the shelf site, andthe vice versa on the upper slope (Sommer et al., unpubl.) thismight enable them to colonize sediments down to 400 m waterdepth. Below 400 m, organic matter degradation, which is pre-dominantly driven by sulfate reduction providing sulfide,decreases (Bohlen et al., 2011), eventually marking the lowerdistribution limit of these bacteria.

4.2. Epifaunal megabenthos

The lower boundary of the Peruvian OMZ at 111S was char-acterized by high densities of epibenthic megafaunal taxa, whichto varying extents are also common across the lower boundariesof OMZs in other regions (Table 4). However, the abundances ofepibenthic organisms off Peru were far higher when compared toother oxygen minimum zones. For instance, the maximum abun-dance of ophiuroids off Peru was 140 ind. m�2 (this study; Levin,2003) compared to abundances of less than 100 ind. m�2 off Chile(Quiroga et al., 2009), 50 ind. m�2 on the California margin(Thompson et al., 1985), 51 ind. m�2 off Oman (Smallwoodet al., 1999), 28 ind. m�2 off Pakistan (Murty et al., 2009), o9ind. m�2 at the Volcano 7, Eastern Tropical Pacific OMZ

Table 4Comparison of epibenthic microbial and megabenthic communities in different OMZ environments.

Region, sampled area,

method

OMZ Edge effect Bacterial mats Main megafauna References

California 300–1400 m

10 box core stations

525–1025 m (O2

o0.5 ml l�1) core 700–

750 m, min. O2 0.27 ml l�1

(�12 mM)

Mentioned at upper

boundary (500–600 m)

Mentioned at 400–500 m Echinoderms: peak near upper (�500 m) and lower edge

(�1200 m), e.g., asteroids (7 ind m�2 at 420 m);

gastropods: peak at 700 m; hermit crabs in core

Hyland et al. (1991),

Levin (2003), Mullins

et al. (1985), Thompson

et al. (1985)

Mexico (Volcano 7)4 parts, 745–3353 m

still image analysis

72–1050 m (O2

o0.5 ml l�1) core 288–

857 m, min. O2 0.09 ml l�1

(�4 mM) at 750 m

Mentioned Pronounced at upper

summit (745–767 m) and

base (2798–3353 m),

reduced at lower summit

(788–857 m) and flank

(1316–1790 m)

Distinct, sometimes overlapping zonation with max.

abundances of poriferans (11 ind m-2 at 770 m, �4 mM),

pennatulaceans (4.3 ind m�2 at 785 m, �4 mM), crabs

(825 m, �6 mM), ophiuroids (860 m, �6 mM); tunicates

and crabs at lower edge

Levin et al. (1991), Levin

(2003), Wishner et al.

(1990), Wishner et al.

(1995)

Peru (121S) 4 coring

stations

170–700 m (O2o0.5 ml l�1) core 200–

400 m, min. O2 0.02 ml l�1

(�1 mM)

Mentioned Mentioned at �300 m, 3–

8 cm sediment depth

Ophiuroids: 140 ind m�2 at lower edge; gastropods at

305 m

Levin et al. (2002), Levin

(2003)

Chile (22, 36, 421S)120–2201 m 9 hauls

on each transect with

50 pictures each

221S: 98–319 m

(O2o0.5 ml l�1); min. O2:

0.06 ml l�1 (� 2.7 mM) at

221S (318 m), 0.45 ml l�1

(�18 mM) at 361S (120 m),

1.28 ml l�1 (�57 mM) at

421S (170 m)

122 m (upper edge) and

363 m (lower edge) at

221S, not off central Chile

Outer shelf (�120 m–

4 mM), up to 10 cm

sediment depth

Echinoderms from �500 m down to 2200 m; crabs

mentioned all over the slope, dominant group at middle

slope (800–900 m)

Gallardo et al. (2004),

Levin (2003), Quiroga

et al. (2009), Sellanes

et al. (2010)

Pakistan (Arabian sea)140–1850 m 5 coring

stations with still

images 27 Agassiz

trawls

140–1300 m (O2

o0.5 ml l�1) core 140–

700 m, min. O2 0.1 ml l�1

(� 4.5 mM), upper

boundary influenced by

Monsoon)

1000–1300 m, abundance

peak at 1000 m

Mentioned Ophiuroids dominant at 1000 m (28 ind m�2, 10–12 mM),

at 1100 m (0.013 ind m�2, �11 mM) together with

holothurians (0.02 ind m�2) and pennatulaceans (0.3 ind

m�2); asteroids only 140–200 m; tunicates dominant

group at 1200 m (87% of megafauna); poriferans at 1200 m

(0.05%) and 1000 m (0.04%); crabs at 140–200 m and

deeper than 940 m; a few gastropods at upper edge;

demersal fish only animals in core

Gooday et al. (2009),

Hughes et al. (2009),

Levin (2003), Levin et al.

(2009), Murty et al.

(2009), Woulds et al.

(2007)

Oman (Arabian sea)400–3400 m 6 coring

stations 3 Agassiz

trawls with images

(827–1254 m)

400–1000 m

(O2o0.5 ml l�1) min. O2

0.13 ml l�1 (� 6 mM) at

400 m

Abundance peak at lower

boundary

Mentioned Narrow band of ophiuroids near lower edge (51 ind m�2 at

1000 m, �10–12 mM); also spider crabs (47 ind m�2) and

galatheids around 1000 m; gastropods common 300–

450 m

Levin et al. (2000), Levin

(2003), Smallwood et al.

(1999)

India (Arabian sea) 540–

2000 m 6 stations, at

all 95 min. video

footage analysed

100–1500 m (O2 o0.5 ml l�1) core 200–

800 m, min. O2 0.35 mM at

540 m

800–1100 m, greatest

abundances at 800 m

[no information] Ophiuroids dominant at 800 m (0.44 ind m�2, �2 mM), at

1100 m (0.037 ind m�2, �15 mM) together with

holothurians (0.015 ind m�2) and asteroids (0.010 ind

m�2); decapods abundant at 800 m (0.15 ind m�2) and at

1100 m (0.037 ind m�2); fish only fauna at 540 m (0.027

ind m�2)

Hunter et al. (2011)

Peru (111S) 80-1030 m

14 video transects with

total length of �23 h,

one picture each min.

50–750 m (O2 o20 mM)

core 200–500 m, min. O2

o2 mM, upper boundary

influenced by O2-

intrusions

460–680 m 80–400 m (O2 o2 mM),

shape patchy-like on the

shelf and thread-like

4300 m

Ophiuriods dominant 580–680 m (max. 140 ind m�2 at

620 m, �5 mM); asteroids 570–700 m (max. 5 ind m�2 at

680 m, �6 mM); tunicates dominant 485-520 m (max. 25

ind m2 at 490 m, o2 mM), also occur 585–685 m (max. 15

ind m�2), co-occur with poriferans; pennaulaceans

exclusive at 540–570 m (max. 20 ind m�2, �4 mM);

gastropods 460–480 m (max. 900 ind m2, o2 mM);

Macrouridae only animals deeper inside core; other fauna

(eel-like fish, anemones, octopods, crabs) observed in

small numbers at lower edge

This study

T.

Mo

schet

al.

/D

eep-Sea

Resea

rchI

68

(20

12

)1

23

–1

35

13

1

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135132

(Levin et al., 1991) or 0.4 ind. m�2 on the Indian margin OMZ(Hunter et al., 2011). Similarly, the maximum abundance of penna-tulaceans off Peru was much higher (20 ind. m�2 at 564 m waterdepth; BW O2 �4 mM) than those reported from Volcano 7 (4 ind.m�2, O2 �4 mM; Wishner et al., 1995) or the Pakistan margin (0.3ind m�2, �11 mM; Murty et al., 2009). This is not surprising as thePeruvian OMZ is linked to the most productive ecosystem in theworld and characterized by the most intense and persistent anoxia(Chavez and Messie, 2009, and references therein). Integratedprimary production off Peru reaches 1.3 kg C m�2 yr�1 (Chavezet al., 2011) compared to 0.6 kg C m�2 yr�1 on the shelf beneaththe California current system (Montecino et al., 2004),0.5 kg C m�2 yr�1 on the Oman margin (Lee et al., 1998) or about0.03 kg C m�2 yr�1 off Pakistan (Schulte et al., 1999). Under non ElNino conditions upwelling is almost persistent throughout the year(Strub et al., 1998). This contrasts with the seasonal variability ofupwelling in other OMZs, for instance in the region off Mauretania(Barton et al., 1998) or monsoon-induced upwelling in the ArabianSea (Reichart et al., 1998).

We analyzed sea-floor images covering the shelf and upperslope on the Peruvian margin at a spatial resolution high enoughto resolve the shape of the distribution patterns of single taxa aswell as overlaps in their distribution. This is in contrast to mostprevious studies of OMZ megafauna, in which the sea floor wasimaged at discrete stations along a depth transect. Prominentzones characterized by different organisms representing differentmodes of feeding, such as suspension- (filter-) feeding, depositfeeding or scavenging, were observed. The spatial overlapbetween these different groups was sometimes small and almostnon-existant, as for example the transition between tunicates andporiferans on one side and pennatulaceans and tunicate larvae orgastropods on the other side. In contrast, the echinodermsdisplayed a rather broad distribution, leading to a wide overlap

Fig. 7. Detailed view on the distribution of selected members (ind. m�2) of the edge co

grey rectangles). Lines indicate respective average abundances for 5 m depth intervals

between the occurence of asteroids, holothurians and ophuiroids(Fig. 7).

As is the case of other OMZs (Levin, 2003; Murty et al., 2009),there was a strong spatial coincidence between these epibenthicmegafaunal communities and the lower boundary of the OMZ.Hence oxygen in addition to organic carbon input, has beenconsidered to be a major parameter controlling their distribution(Levin et al., 1991; Levin, 2003; Levin et al., 2009). By imposingspecies-specific physiological constraints, BW oxygen certainly setsthe limit to which these megafaunal species can invade the OMZ inorder to access enhanced concentrations of organic matter. How-ever, the small-scale distribution of the different taxa may also beinfluenced by other structuring factors. The epibenthic megafaunaoften occurs in a narrow depth range of o100 m, across which thechange in BW oxygen levels is only 4 mM at most (Murty et al.,2009; Wishner et al., 1990), representing a depth-related oxygengradient of 0.02 to 0.04 mM m�1. Such a small change in oxygenlevels is unlikely to have major effects on the distribution of theseepibenthic communities. We found poriferans and tunicates occur-ring at several depths within the lower boundary leading to theconclusion that such an oxygen gradient has only a minor influenceon the small-scale structure of these edge communities. Our dataindicate that the BW current and turbulence regime representsanother important factor governing the availability of POM in thebenthic boundary layer and thus the distribution of epibenthicmegafaunal communities.

4.3. Hydrodynamic controls on the distribution of epibenthic

megafauna

Following the concept suggested by Frederiksen et al. (1992;see also Fig. 11.12 in Gage, 2003), we hypothesise that the

mmunity in relation to turbidity (FTU) and critical slope areas (marked with dark

.

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135 133

distribution of benthic filter-feeding communities is a function ofinternal waves breaking on the continental slope. For particularconditions of water-column stratification and certain continentalslope angles, internal waves locally dissipate their energy, resultingin enhanced bottom shear-stress. This causes high levels of sus-pended particles that lead to the formation of nepheloid layers(Cacchione and Drake, 1986; Garrett and Gilbert, 1988). Under lowcurrent velocity conditions, particles will settle out of these layersand provide food to the filter-feeding community immediatelybelow. Such a mechanism has been also used to explain thedistribution of the coral Lophelia pertusa and large demospongids(Frederiksen et al., 1992; Klitgaard et al., 1997), filter-feedingophiuroids round the Faroe Islands NW-Atlantic (Tyler et al.,2005), and the distribution of the hexactinellid sponge Pheronema

carpenteri at 1000 m water depth in the Porcupine Seabight (Riceet al., 1990). The effect of near-bottom water currents and turbu-lences on the deposition, re-suspension and transport of particlesand consequently on the availability of POM at the Namibian Shelfhas been further described by Monteiro et al. (2005).

As mentioned above, the energy dissipation of internal wavesat the continental margin is affected by the relative slope of thesea floor (a) and the slope of internal wave propagation (b), whichis set by the local stratification, the Coriolis force and the internalwave frequency. Upon reflection, internal waves preserve theirangle to the horizontal rather than to the reflecting surface(Phillips, 1977). As a result, reflection from slopes near the criticalangle leads to enhanced vertical shear of horizontal internal wavevelocities, which results in turbulence and enhanced bottomshear stress. For subcritical conditions, the energy of internalwaves is reflected up-slope. As in the case of critical conditions,the wavelength of the reflected wave will be reduced compared tothe incident wave, accelerating BW velocities and intensifyingbottom shear stress. Such conditions can impede settlement offine-grained material and lead to the development of bottomnepheloid layers, thus controlling the deposition of sediment inshallow waters (Cacchione and Drake, 1986). Under supercriticalconditions, internal wave energy is reflected back into the ocean.In fact, overall continental slope morphology may be controlledby internal tides (Cacchione et al., 2002).

Distinct zones along the investigated transect off Peru wereidentified as having the potential to become critical. We did notdirectly measure fine-scale BW velocities or turbulences. How-ever, across-slope distribution patterns of sedimentological para-meters such as grain size, the ratio between Zr and Al, and the Corg

content in the surface sediments, indicate increased bottom shearstress in these potentially critical areas, leading to sediment re-working and particle re-suspension. As Zr is heavier than Al, it ismobilized at higher BW turbulences than Al (Ganeshram et al.,1999; Boning et al., 2004). Hence the Zr/Al-ratio becomes ele-vated under these hydro-dynamic conditions, as at our 512-m-site (MUC 40), which furthermore was associated with a very lowsedimentation rate of 20 cm kyr�1. The distribution of sand andsilt along this transect further indicates sediment re-working. Asexpected, an increase in the sand content was positively corre-lated with an increase of the Zr/Al-ratio. Elevated turbidity wasassociated with these potentially critical sites and small-scalechanges of the sea floor topography. Enhanced turbidity inregions (80, 200 and 340 m water depth) that were not classifiedas critical might have other causes. Bottom shear stress may beenhanced here as a result of elevated Ekman velocities in thebottom boundary layer associated with the presence of the PUCand Peruvian Coastal Current in the water column above (e.g.,Siedlecki et al., 2012). Additionally, coastal trapped waves that areoften observed propagating poleward along the coast of Peru (e.g.,Smith, 1978), may contribute to enhanced currents in the near-bottom layers.

The locations at which the margin becomes critical or near-critical coincide very well with the distribution of megafaunaltaxa, particularly echinoderms but also tunicates and poriferans(Fig. 7). Between 485 and 520 m tunicates and poriferans, as wellas patches of large arborescent foraminifera (Pelosina sp.), repre-sent the dominant epibenthic megafaunal groups, although theytend to avoid a narrow zone around 510 m that was associatedwith a distinct turbid plume. Above �485 m, the BW hydrody-namic regime seems to become unfavorable for the gastropods(Astyris permodesta) that penetrated deepest into the OMZ. Asgrazers, these gastropods depend on low BW current velocitiesand low turbulences, conditions that allow the deposition of POM.Due to their small body size, they may be more able to tolerateoxygen deficiency than larger organisms (Levin et al., 1991)allowing them to invade deeply into the OMZ. In addition, Levin& Michener (2002) concluded from isotopic signatures ofA. permodesta that these gastropods probably feed on filamentoussulfur bacterial mats at methane seeps at the coast of Oregon andNorth California. Thus, the gastropods and spionid polychaetesmay be able to invade deeply into the OMZ as a result of theircapability to meet their energy requirements by anaerobic meta-bolism (Gonzalez and Quinones, 2000; Levin, 2003; Quiroga et al.,2007). A similar mechanism has been suggested to explain thehigh tolerance of hypoxia exhibited by several shallow-watermacrobenthic organisms such as Sipunculus nudus or Arenicola

marina (Grieshaber et al., 1992). A. permodesta has also beenreported from the centre of the Santa Barbara Basin (Bernhardet al, 2003). Large numbers of another gastropod, Tibia delicatula,

were encountered inside the core of the Oman OMZ (Goodayet al., 2009). This species was sporadically present at the upperedge of the Pakistan OMZ (Ramirez-Llorda and Olabarria, 2005).At these sites, the O2 concentrations were46 mM which is higherthan the oxygen levels of o2 mM observed in the habitat ofA. permodesta during the present study.

In the oxygen-deficient waters of the California BorderlandBasins, Oman and Peru the suspension-feeding foraminiferaPelosina sp. has been observed to extend up to 4 cm from thesediment surface into the BW (Gooday et al., 2000; Gooday et al.,2009). Their spatial distribution in these areas indicates that theseorganisms cannot tolerate BW O2 levels o�9 mM (Gooday et al.,2000). However, the distribution patterns described in this studysuggest that this tolerance threshold is as low as �2 mM. Fieldstudies on the Swedish west coast, as well as laboratory experi-ments, demonstrate that P. arborescens can survive anoxic condi-tions for at least 10 days (Cedhagen, 1993).

Abundant tunicates and poriferans were also present in waterdepths ranging from 585 to 685 m, another critical area that ischaracterized with two turbid plumes at its upper boundary(Fig. 7). As in the critical area at 510 m water depth, the tunicatesseem to avoid areas of strongly enhanced particle load in thewater column (Fig. 7). In the depth range of 585 to 685 m, sandysediments with high amounts of carbonates were sampled andsmall lumps of phosphorites, which could serve as hard substratefor colonization, were recovered during a lander deployment(BIGO-T2, 594 m). The presence of widespread hard grounds wasalso evident in the sea-floor images. The ophiuroids that stronglydominated the echinoderm community were clearly concentratedat 620 m water depth, marking the upper boundary of the regionwhere the slope becomes critical and showed a pronounced dip inthe sea-floor topography. Consistent with the hypothesis proposedby Tyler et al. (2005), the ophuiroid peak was located immediatelybelow a well-developed turbid layer but still within another lesspronounced one (Fig. 7). The distribution of abundant ophiuroidsnorth of Iceland (Piepenburg and Juterzenka, 1994), on the NW-Scottish margin (Lamont and Gage, 1998), and in the NortheastChannel on the Canadian continental slope off Nova Scotia

T. Mosch et al. / Deep-Sea Research I 68 (2012) 123–135134

(Metaxas and Giffin, 2004), were apparently related to increasedcurrent velocities and breaking internal waves causing differentpatterns of food supply for the benthos.

In contrast to the ophiuroids, the deposit-feeding asteroids andalso holothurians, presumably Psolus sp., have been observed ingreater water depth within this critical region, which is charac-terized by low bottom-water turbidity levels. Psolid holothurianshave also been reported sporadically at 121S off Peru in 602 mwater depth (Resig & Glenn, 1997), as well as at the lower edge ofthe Pakistan OMZ (Gooday et al., 2009). Different species ofholothurians were observed to occur at a wide range of BW O2

levels in the Gulf of California off Mexico (Massin & Hendrickx,2011). In this area, Psolidium gracile was penetrating deepest intothe OMZ and occurred at O2 levels o2.2 mM.

As suggested by Frederiksen et al. (1992) and Gage (2003),these asteroids and holothurians might benefit from particleexport from the nepheloid layers that were observed at 580 and620 m (Fig. 7). Similarly, crustaceans, present at the lower dis-tribution limit of the entire edge community, might also benefitfrom this particle deposition. Pennatulaceans protrude from thesediment surface into the BW where they depend on suspendedPOM. Unexpectedly, these organisms were present only in regionsthat were identified as subcritical and associated with lowturbidity. Flow-tank experiments showed that the filtering effi-ciency of the pennatulacean Ptilosarcus gurneyi was reduced withincreasing current velocity (Best, 1988), suggesting that theseorganisms may avoid strong BW turbulence and current regimes.

By imposing species-specific physiological constraints, the BWO2 concentration set the upper distribution limit for the epi-benthos to invade into the OMZ. However, the factors controllingtheir lower, rather abrupt distribution limit remained unclear.The decline of epifaunal abundances below 680 m was in contrastto a rather gradual decline of the overall food supply (Sommeret al., unpubl.) and to an increase of BW O2. Beside Corg input andthe presence of more refractory organic material, as indicated byhigh C/N-ratios, this might represent a community response to theboundary between two water masses, the AAIW and the PDW(Silva et al., 2009), as also observed off Chile (Palma et al., 2005).

Acknowledgements

We thank the officers and the crew of RV ‘Meteor’ duringcruise M77-1/2. We are grateful for B. Bannert for his supportwith the video and imaging technique. Many thanks are due toK. Kroger, A. Thurber and A. Waren for their great help withregard to taxonomy and species identification. We thankM. Dibbern, B. Domeyer, S. Kriwanek and R. Ebbinghaus forhelping with the geochemical analyses. We also thank R. Schulzfor measuring 210Pb; R. Duttmann, D. Garbe-Schonberg, P. Appeland D. Rau for assistance in sediment analysis and XRF measure-ments; as well as C. Dos Santos Ferreira for the processing ofmultibeam data. We are very grateful for the insightful commentsand suggestions by A. Gooday and 2 anonymous reviewers, whichgreatly improved the manuscript. This work is a contribution ofthe Sonderforschungsbereich 754 ‘‘Climate - BiogeochemistryInteractions in the Tropical Ocean’’ (www.sfb754.de) which issupported by the Deutsche Forschungsgemeinschaft.

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