Porewater nutrient concentrations and benthic nutrient fluxes across the Pakistan margin OMZ

ARTICLE IN PRESS Deep-Sea Research II 56 (2009) 333–346

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Deep-Sea Research II journal homepage: www.elsevier.com/locate/dsr2

Porewater nutrient concentrations and benthic nutrient fluxes across the Pakistan margin OMZ Clare Woulds a,, Matthew C. Schwartz a,1, Tim Brand b, Greg L. Cowie a, Gareth Law b,2, Stephen R. Mowbray a a b

School of GeoSciences, The University of Edinburgh, Edinburgh EH9 3JW, Scotland The Scottish Association for Marine Science, Dunstaffnage Marine Laboratory, Oban PA37 1QA, Scotland

a r t i c l e in fo

abstract

Article history: Accepted 31 May 2008 Available online 5 November 2008

Porewater concentrations and benthic fluxes of phosphate, silicate, ammonia, nitrate and nitrite were measured at five sites spanning the Pakistan margin oxygen minimum zone (OMZ), in order to characterise the biogeochemical processes occurring, and to assess whether oxygen concentration and a seasonal pulse of organic matter are controlling factors. Typical concentrations of 1–70 mM, 50–250 mM, +   0–270 mM, o5 mM and 0–4 mM for PO3 4 , H4SiO4, NH4, NO3 and NO2 , respectively were obtained. onto iron and Evidence was found for the occurrence of intense denitrification, sorption of PO3 4 manganese oxyhydroxides and possibly fluoroapatite precipitation at depth (430 cm) in the sediment. These processes are all redox-sensitive, and their intensities varied across the margin, suggesting that oxygen concentration exerts a strong influence over nutrient concentrations and cycling. Variation in nutrient concentrations and fluxes before and after the summer monsoon was limited to an oxygendriven change to the PO3 4 profile at one site, indicating that either nutrient profiles do not generally alter on seasonal timescales, or that any impact of the monsoon had subsided before the post-monsoon sampling period. Porewater profile modelling tended to underestimate the magnitude of fluxes, but was in general agreement with the directions of measured fluxes, and in situ and shipboard flux measurements also generally agreed. Phosphate and H4SiO4 concentrations and benthic fluxes on the Pakistan margin were similar to those reported at abyssal sites from around the world, while NH+4 and NO 3 concentrations and fluxes were comparable to shallower, more productive and/or hypoxic marine settings. & 2008 Elsevier Ltd. All rights reserved.

Keywords: Nutrients Porewater Benthic flux Oxygen Minimum Zone Denitrification Arabian Sea

1. Introduction When organic matter is deposited in marine sediments it undergoes decay, during which inorganic nutrients are released into the porewaters, typically resulting in elevated concentrations and outward fluxes into overlying waters. However, other processes, such as denitrification and authigenic phosphogenesis, create a potential for reverse benthic fluxes (i.e. into the sediments). Ultimately, sedimentary processes, as either source or sink terms, may serve as important controls on ocean nutrient  Corresponding author. Current address: School of Geography, University of Leeds, Leeds LS2 9JT, United Kingdom. E-mail addresses: [email protected], [email protected] (C. Woulds), [email protected] (M.C. Schwartz), [email protected] (T. Brand), [email protected] (G.L. Cowie), [email protected] (G. Law), [email protected] (S.R. Mowbray). 1 Current Address: Department of Environmental Studies, University of West Florida, Pensacola, USA. 2 Now at: School of Earth & Environment, Institute for Geological Sciences, Environment Building, The University of Leeds, Leeds LS2 9JT, UK.

0967-0645/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr2.2008.05.034

inventories, surface ocean productivity, drawdown of atmospheric CO2, and, potentially, climate (e.g., Ganeshram et al., 1995, 2000). Studies of nutrient distributions in marine sediments have been used to provide insight into the rates and paths of organic matter remineralisation, and to link this to regional patterns of surface water productivity, whole-basin nutrient budgets and microbial process rates. Grandel et al. (2000) for example found that nutrient regeneration in abyssal Arabian Sea sediments was closely linked to productivity and the amount of organic matter reaching the sediment, and Rasheed et al. (2006) found that nutrient release from sediments of the Gulf of Aqaba was sufficient to sustain all of the primary productivity in the region. In addition, comparisons of the release rates of different nutrients with both the Redfield ratios, and with fluxes of dissolved oxygen and dissolved inorganic carbon have been used to indicate the relative rates of aerobic respiration, nitrate reduction and iron and manganese reduction (e.g., Hopkinson et al., 2001; Jahnke et al., 2005). Therefore, nutrient profiles and benthic fluxes provide vital information on the biogeochemical functioning of marine sediments, and their quantification is essential for our understanding

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of global ocean nutrient budgets, productivity, organic carbon burial and climate. Despite this, direct determinations of benthic nutrient fluxes have been comparatively few in number (especially in situ). Furthermore, benthic biogeochemical processes (including bioturbation and irrigation, which can influence nutrient fluxes), are potentially affected by a variety of environmental factors and site conditions. There have been few if any systematic comparative studies that have encompassed wide depth ranges, seasons of contrasting productivity, and sites with contrasting redox conditions and benthic communities. As a result, much remains to be learned about the magnitude, direction and environmental controls of benthic nutrient fluxes. Pakistan margin sediments are impacted by the Arabian Sea oxygen minimum zone (OMZ). This is a layer of water between 150 m and 1000 m depth where oxygen concentrations are permanently low, and which is responsible for over one quarter of the world’s naturally hypoxic seafloor (Helly and Levin, 2004). Globally, OMZs are important regions for organic carbon burial (De Maison and Moore, 1980), and have recently been implicated as the driving forces behind global nitrogen fixation (Deutsch et al., 2007). Therefore, the Arabian Sea OMZ is potentially of global significance in ocean nutrient budgets. The steep gradients in bottom-water dissolved oxygen concentration produced by the Pakistan margin OMZ are accompanied by similarly steep gradients in sediment organic matter content and benthic community composition. Thus the biogeochemical regimes encountered on the Pakistan margin (in terms of depth, sediment organic matter content, benthic redox conditions, biological communities, and both microbial and faunal processes) are more diverse and complex than those previously studied. Further, the monsoon-driven upwelling, productivity, and increase in organic matter flux to the seafloor which occurs twice a year in the Arabian Sea (Haake et al., 1993) allows investigation of the response of nutrient dynamics to an organic matter pulse. The objectives of this study were to characterise porewater nutrient profiles and benthic nutrient fluxes at sites spanning the Pakistan margin, before and after the summer monsoon, in order to address the following questions: (1) What biogeochemical processes are active on the Pakistan margin, and how do these vary between sites with contrasting oxygen and organic matter concentrations? (2) To what extent does oxygen concentration influence nutrient porewater concentrations, profiles and benthic fluxes? and (3) Does the summer monsoon have an impact on nutrient concentrations and fluxes? In addition, consideration is given to the relative merits of estimating benthic nutrient fluxes via modelling of porewater profiles versus direct measurement, both in situ and shipboard, using recovered samples. This work fits into a wider study of sediment geochemistry, benthic communities and biogeochemical processes on the Pakistan margin, and thus forms part of a detailed look at variation across an OMZ.

able) site. Sediment organic matter contents showed maximal values roughly coincident with the lower OMZ (3.4 wt% at 940 m), and minimal values at the deep, oxygenated 1850 m site (1.3 wt%, Cowie et al., 2009). The composition and biomass of the benthic communities at our study sites also varied with oxygen availability, with burrowing metazoan macrofauna present at the 140, 940, 1200 and 1850 m sites (Hughes et al., 2009) and maximal biomass in the lower OMZ, (Levin et al., 2009). Metazoan macrofauna were almost absent at 300 m within the OMZ core, where foraminifera dominated the community (Larkin and Gooday, 2009; Gooday et al., 2009; Hughes et al., 2009). Sediment X-radiographs showed fully bioturbated sediment at the 140, 1200 and 1850 m sites, and discrete burrows with preserved laminations at the 940 and the 300 m sites (Hughes et al., 2009). Sampling was conducted on four cruises. Cruises CD 145 and CD 146 occurred during the inter-monsoon period (March–May) preceding the summer (SW) monsoon of 2003, and cruises CD 150 and CD 151 occurred afterwards (August–October), in the latemonsoon and post-monsoon periods. The only major environmental change observed at the study sites between the inter- and post-monsoon sampling seasons was a decrease in water-column oxygen concentration (71–1 mM) at the 140 m site. This decrease was attributed to a shoaling of the upper edge of the OMZ (see, Brand and Griffiths, 2009; Breuer et al., 2009, for further discussion). 2.2. Sediment sampling Sediment cores (10 cm i.d.) were retrieved with a Bowers and Connelly multiple corer and transferred immediately to a controlled temperature laboratory set to in situ temperature. They were sectioned at intervals of 0.5–10 cm depth, then 1–20 cm depth and at 2 cm intervals thereafter to the bottom of the core (usually 30 cm) under a nitrogen atmosphere. Porewaters were extracted by centrifugation, filtered to 0.2 mm (with Asypore cellulose acetate filters), and stored refrigerated (no longer than 1 day) prior to analysis. Occasionally problems were encountered  with NO 3 and NO2 analyses while at sea (due to instrument problems or contamination). Gaps in the data were filled by analysing samples that had been collected in the same way and then frozen (at 20 1C) during transit to the UK. It is recognised that this is not ideal, but it remains preferable to missing data. In addition to the nutrient profiles from the five study sites, five replicate profiles were produced from an additional site at a depth of 700 m during cruise CD 150. Three of the profiles are derived from a triplicate set of cores retrieved from one corer deployment, and the other two profiles are derived from cores retrieved on a subsequent deployment. This was done in order to assess small-scale spatial heterogeneity (courtesy of T. Shimmield). 2.3. Core incubation studies

2. Methods 2.1. Study area The study was conducted at five stations comprising an offshore transect of the Pakistan continental margin (see Table 1 for site coordinates). The station depths (140, 300, 940, 1200 and 1850 m) spanned the depths where an OMZ impinges on the seafloor (150–1000 m), thus dissolved oxygen concentrations varied from relatively well oxygenated at the 1850 m (85 mM), 1200 m (12 mM) and 140 m sites (71 mM), to poorly oxygenated at the 940 m (2.5 mM) and especially the 300 m (oxygen undetect-

Nutrient flux determinations were carried out via incubations of whole, undisturbed sediment cores (10 cm i.d.) with overlying waters during CD146 and CD151. Cores were sealed and kept at in situ temperature (but atmospheric pressure), in the dark, for 4 days. During this time, overlying waters (1.4 L) were stirred, and oxygen levels were maintained at ambient seafloor concentrations using an ‘‘oxystat’’ system, that circulated the water through gaspermeable tubing placed in a reservoir of seawater at fixed oxygen concentration (M. Schwartz, unpublished data). Overlying waters were sampled at the start of each incubation, and at 24 h intervals thereafter. This sampling frequency, combined with the oxystat system allowed us to evaluate nutrient fluxes over relatively long

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Table 1 Site locations and conditions. Site (equals water depth in m)

Latitude (N)

Longditude (E)

Temperature (1C)

Dissolved oxygen concentration (mM)

140 300 940 1200 1850

23.16.53 23.12.30 22.55.00 23.00.00 22.52.25

66.42.47 66.33.46 66.36.19 66.24.18 66.00.10

18–22.5 14.5–16.5 9–9.5 7 3.5–4

70.5 (1.0 post-monsoon) Undetectable 2.0–2.9 10.6–14.1 80.4–89.3

Temperature data are ranges from multiple CTD deployments during both pre- and post-monsoon seasons. Dissolved oxygen data are from Breuer et al. (2009) and are derived from samples collected by the benthic lander.

periods of time. Nutrient accumulation during incubations is not thought to have been sufficient to have inhibitory effects on the benthic community. Each incubation was conducted simultaneously on two cores. The incubation at the 940 m site during CD 146 was unsuccessful due to sample loss. In situ benthic flux incubations were conducted during cruise CD 151 using a benthic lander fitted with an ELINOR chamber (surface area sampled 0.09 m2) (Glud et al., 1995; Black et al., 2001), and employed the use of stirring, an oxystat system and time-series water sampling, just as for the shipboard equivalents. 2.4. Analysis The incubation and porewater samples were analysed on a Lachat Quick Chem 8000 flow injection autoanalyser using Lachat methods 31-107-06-1-B (ammonia) 31-107-04-1-A (nitrate and nitrite), 31-115-01-I (orthophosphate) and 31-114-27-1-A (silicate). Porewater samples were subject to eightfold dilution prior to analysis. Salt refraction effects for both porewater and incubation samples were removed by re-running a representative number of samples with one critical reagent in each method replaced with Milli-Q water. Salinity blank responses were  negligible, except for where very low NO 2 and NO3 concentrations were found, in which case blank corrections resulted in values close to zero. 2.5. Flux calculations Measured benthic nutrient fluxes were determined from incubation time-series concentration data by the fitting of lines of best fit. This process was complicated by the fact that simple linear increases or decreases in concentration were not always observed in the experimental chambers (shipboard or in situ). When single data points deviated significantly from otherwise clear trends these were excluded from flux calculations. Occasionally, nutrient concentrations changed in one direction for up to 2 days, and then followed the reverse trend for a similar amount of time. This has been observed previously by Devol and Christensen (1993), who suggested that a biogeochemical change in the incubation chambers may have resulted from the incubation process. In this study the phenomenon was most common in  the case of NH+4, NO 2 and NO3 , and therefore implied a change in nitrogen cycling within the incubation chambers. In such cases, only the early (first 2 days, pre-alteration) parts of the curves were used to calculate fluxes. It is stressed, however, that this action was necessary in o20% of flux calculations. For shipboard studies, fluxes were calculated separately for each experimental chamber, and average values are reported. Modelled fluxes were derived from porewater profiles using the code ‘Profile’ (Berg et al., 1998). The model input parameters were: porewater solute concentration with depth, porosity, and the respective solute molecular diffusion coefficients. Nutrient diffusivities were obtained from Schulz and Zabel (2006), and

Table 2 Modelled nutrient fluxes in mmoles m2 d1. 140

300

940

1200

1850

Phosphate CD 145 CD 146 CD 150 CD 151

– 0.008 0.034 0.072

0.022 0.002 0.003 0.018

– – 0.001 0.014

0.001 – 0.002 0.001

–0.0004 0.0002 0.0003 0.002

Silicate CD 145 CD 146 CD 150 CD 151

– 0.086 0.063 0.299

0.107 – 0.026 0.108

– – 0.055 0.078

0.001 – 0.091 0.005

0.052 0.053 0.109 –

Ammonia CD 145 CD 146 CD 150 CD 151

– 0.082 0.126 0.207

0.201 0.142 0.116 0.130

– 0.073 0.071 0.060

0.020 0.003 0.076 0.010

0.143 0.011 0.080 0.263

Negative values indicate fluxes into the sediment. The symbol ‘–’ indicates sites and cruises from which the data were unsuitable for profile modelling. This was due to short cores, scattered data that produced a very poor model fit, and the fact that the 140 and 940 m sites were not visited during CD 145. Nitrate and nitrite profiles were not suitable for flux modelling.

corrected for the bottom-water temperature at each site (Li and Gregory, 1974). The boundary conditions used were the nutrient concentrations at the top and bottom of the profiles (option 1); and the sediment diffusivity (Ds) of each nutrient was expressed as Ds ¼ j2D (option 2), where j is the porosity, and D is the nutrient diffusivity in free water. Sediment porosity data were obtained from sediment wet/dry weights. Biodiffusion and irrigation coefficients were not provided to the code ‘Profile’; therefore, the resultant fluxes are due to diffusion alone. The model estimates the net rate of solute production/consumption at each depth through an optimisation procedure. A series of possible fits are compared through statistical F testing. The simplest consumption and/or production profile that reproduces the concentration profile is given as the output, along with a benthic flux value. We aimed to model all four porewater profiles (one from each cruise) for each nutrient at each site. Table 2 shows when modelling of a particular profile was not possible due to lack of data or scatter in the data. Modelled fluxes of NO 2 and NO 3 are not presented, as almost all of the profiles obtained were unsuitable for modelling.

3. Results 3.1. Porewater profiles Data from all four cruises have been plotted on the same graph for each site and nutrient. Phosphate concentrations showed a

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Phosphate (µM) 0

0

20

40

60

Phosphate (µM) 80

0

CD 145

10

CD 146

0

20

40

60

Phosphate (µM) 80

0

10

10

20

20

0

20

40

60

80

30

Depth (cm)

CD 151

20

Depth (cm)

Depth (cm)

CD 150

30

40

40

40

140 m

50

300 m

50

Phosphate (µM) 20

40

60

0

10

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940 m

Phosphate (µM) 80

Depth (cm)

Depth (cm)

0

0

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0

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40

1200 m

50

1850 m

Fig. 1. Porewater phosphate concentrations. The apparently anomalous profiles from CD 146 at the 300 and 940 m sites are not included in the interpretation.

range of 1–70 mM, with considerable variation both down-core and between sites (Fig. 1). At the more hypoxic 300 and 940 m sites, PO3 4 concentrations increased from low values (o10 mM) at the sediment–water interface to sub-surface peaks of 50–70 mM at 8 cm depth. Below this, they declined. Concentrations at the more oxygenated sites (140, 1200 and 1850 m) were roughly constant with depth and lower (o10 mM). Notably, after the monsoon the 140 m site showed a profile similar to the hypoxic sites. Porewater silicate concentrations (Fig. 2) in surface sediments increased slightly across the margin from 50 to 70 mM at the 140 and 300 m sites to 200 mM at the 1850 m site. Concentrations increased slightly down-core, and that increase was greater at the deeper sites (Fig. 2). In addition the 140 m site showed sub-surface silicate peaks, at 2 cm depth. At the 140, 300, 940 and 1200 m sites, ammonia concentrations were low (0–30 mM), and increased with depth in the sediment (Fig. 3). Maximal down-core concentrations (250–270 mM)

occurred at the 140 and 300 m sites. The 1850 m site showed lower concentrations (10–70 mM) and a differently shaped profile. Concentrations decreased from the surface to 3 cm depth, below which they gradually increased. Nitrite concentrations were usually o1 mM, except for subsurface peaks at the 300 and 940 m sites, and at the very surface of the 1200 m site, where they were as high as 4 mM (Fig. 4). The 1850 m site showed higher surface values of 21–37 mM, decreasing to an almost undetectable level by 1.5–2 cm depth. Nitrate was only reliably detected in the surface 2 cm of sediments, in concentrations typically o5 mM (Fig. 5). Occasionally, however (e.g., at the 140 and 300 m sites during CD145, and at the 940 m site during CD 151), very high surface and subsurface values were measured (see Fig. 5). A similar problem is also evident in the NO 2 data (in CD 151 cores from 300 and 940 m, see Fig. 4). These anomalously high results must be treated with care. Oxidation of ammonia, which is comparatively abundant in Pakistan margin porewaters, has been known to contaminate NO 3

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Silicate (µM) 100

200

0

CD 145 CD 146 CD 150 CD 151

Depth (cm)

10

Depth (cm)

Silicate (µM) 300

20

30

100

0

140 m

50

10

20

20

30

100

200

100

200

300

30

300 m

50

940 m

Silicate (µM) 300

0

10

10

20

20

30

0

40

50

Depth (cm)

Depth (cm)

0

0

10

Silicate (µM) 0

100

200

300

30

40

40

50

Silicate (µM) 300

40

40

0

200

Depth (cm)

0

0

337

1200 m

50

1850 m

Fig. 2. Porewater silicate concentrations. The apparently anomalous profile from CD 146 at the 940 m site is not included in the interpretation.

data (Berelson et al., 1990). This is particularly suspected as porewaters were diluted with oxygenated water prior to analysis. However it should be noted that small-scale heterogeneity could also have caused some within-site variation and profile spikiness.  On balance it seems likely that unexpectedly high NO 3 and NO2 values were the product of contamination, and they are not included in the interpretation. The only site to show reproducible high NO 3 concentrations was the 1850 m site, where values up to 40 mM were found at the sediment–water interface. Fig. 6 shows the down-core nutrient profiles from the five replicate cores taken at an additional site at 700 m water depth during cruise CD 150. For all parameters, the five profiles are very similar. While the 700 m site showed an almost complete absence of macrofauna, and could therefore be more spatially homogenous than other sites, it is still felt that the observed reproducibility of profiles justifies the use of a single core profile from each of four cruises at the main study sites. In a few cases (NH+4 and PO3 4 at at 300 m, and Si at 940 m) concentrations from the 140 m, PO3 4 CD 146 cruise were anomalously low (Figs. 1–3), apparently due to

analytical problems; these data are not included in our interpretation.

3.2. Nutrient fluxes 3.2.1. Modelled fluxes Modelled fluxes are presented in Table 2 and in Fig. 7. The values plotted in Fig. 7 are averages of all those presented in Table 2 for each nutrient at each site, i.e. the averages are from data collected on all four cruises. As neither porewater profiles nor modelled fluxes showed systematic seasonal variation, this averaging across seasons is considered appropriate. Modelling of porewater profiles suggested outward fluxes of + PO3 4 , H4SiO4 and NH4 (Fig. 7), and therefore that sediments are sources of these nutrients to the water column (except at the + 1850 m site where they were a sink for PO3 4 and NH4). Fluxes of 3 + PO4 , H4SiO4 and NH4 generally decreased with increasing site water depth (with an anomalously low H4SiO4 value at the 1200 m

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Ammonium (µ µM) 100

Ammonium (µM) 300

0

CD 145 CD 146 CD 150 CD 151

10

20

Depth (cm)

Depth (cm)

200

30

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140 m

50

0

10

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100

200

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300

30

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300 m

50

50

940 m

Ammonium (µM) 300

0

0

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Depth (cm)

10

Depth (cm)

Ammonium (µM) 300

10

Ammonium (µM)

20

30

20

30

40

40

50

200

40

40

0

100

Depth (cm)

0

0

1200 m

50

1850 m

Fig. 3. Porewater ammonium concentrations. Note the different x-axis scale for the 1850 m site. The apparently anomalous profile from CD 146 at the 140 m site is not included in the interpretation.

site), turning sediment effluxes to sediment influxes at the 1850 m and NH+4. Unfortunately the scatter site in the cases of PO3 4  present in down-core NO2 and NO 3 data meant that it was not possible to produce a good-quality fit of the model to the data.  Therefore modelled NO 2 and NO3 fluxes are not presented. Measured fluxes are shown in Table 3, and are plotted alongside modelled fluxes in Fig. 8. In most cases, shipboard and in situ lander measurements showed reasonable agreement in and H4SiO4 terms of magnitude and direction. Measured PO3 4 fluxes out of the sediment were maximal at the 140 and 300 m sites and minimal at the 1850 m site. Conversely, large fluxes of both of these nutrients into the sediment were measured at the 940 m site. Ammonium fluxes measured via shipboard experiments were into the sediment, and became less with increasing station depth, until fluxes out of the sediment were measured at the 1850 m site. However, in situ measurements via benthic lander incubations showed strong fluxes of NH+4 out of the sediment at the 140 and 300 m sites. Nitrite was observed to flux out of the sediment at all except the 300 m site (maximal efflux at the 940 m

site). Nitrate was observed to flux into the sediment at all except the 1850 m site, and maximal values were coincident with the OMZ (the 300 and 940 m sites).

4. Discussion 4.1. Data quality A brief consideration of the reasons for anomalies in the data will be given first. fluxes into the sediment in Apparently anomalous PO3 4 shipboard measurements (Fig. 8) may have been due to temporary oxygenation of cores during incubation set-up. This would have allowed formation of Fe oxyhydroxides, to which PO3 4 is known to adsorb (van Raaphorst and Kloosterhuis, 1994), thus providing a PO3 4 sink in the sediment. Similarly, oxygen contamination could have caused measured influxes of NH+4 at sites where porewater profiles strongly suggested effluxes. Oxygenation could have

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Nitrite (µM)

Nitrite (µM) 8

0

CD 145 CD 146 CD 150 CD 151

0

4

0

10

20

20

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30

Depth (cm)

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40

140 m

50

0

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300 m

50 4

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Depth (cm)

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8

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940 m

Nitrite (µM) 8

10

30

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40

µM) Nitrite (µ

Depth (cm)

Nitrite (µM) 8

10

Depth (cm)

Depth (cm)

0

4

0

339

20

0

40

30

40

1200 m

50

1850 m

Fig. 4. Porewater nitrite concentrations. Note the different x-axis scale at the 1850 m site. The scattered data and high values at the 300 and 940 m sites may be the result of ammonium oxidation during sampling, and are excluded from the interpretation.

stimulated nitrifying bacteria, which would consume NH+4. At the 300 m site on cruise CD 146 this would also explain the anomalous + efflux of NO 2 (Fig. 8). In support of this suggestion, NH4 concentrations tended to increase during the late stages of shipboard incubations at the 300 and 940 m sites (data not shown), possibly indicating a recovery from oxygen contamination and a return to normal function. It should also be noted that NH+4 profiles, and therefore modelled fluxes, may have been affected by changes in the solid/dissolved partitioning of NH+4 during decompression (Berelson et al., 1990 and references therein). It is relatively unsurprising that where oxygen contamination of shipboard experiments was suspected, the shipboard measured fluxes tended to deviate from in situ measurements. At these, usually low oxygen sites, in situ measurements are therefore more reliable than shipboard measurements. Where oxygen contamination of shipboard experiments was less likely, the two measurement methods generally produced fluxes of similar magnitude (Fig. 8).

4.2. Oxygen and biogeochemical processes Cross-margin patterns of nutrient profiles and fluxes showed a clear impact of low oxygen on nutrient cycling. Phosphate profiles at the 300 and 940 m sites, and at the 140 m site in the postmonsoon season (when conditions were hypoxic) showed subsurface maxima and higher concentrations than those at the more oxygenated 1200 and 1850 m sites (Fig. 1). Phosphate is thought to readily associate with particulate Fe and Mn (van Raaphorst and concentrations at Kloosterhuis, 1994), and high porewater PO3 4 hypoxic sites may be linked to PO3 4 release upon the microbially mediated reductive dissolution of Fe and Mn oxyhydroxides. Indeed the seasonal increase in PO3 4 concentration at the 140 m site was commensurate with strong Fe3+ and Mn reduction (Law et al., 2009). Low PO3 4 concentrations at oxic sites may be due to to metal oxides. The increased sorption of dissolved PO3 4 concentrations below sub-surface peaks decreases in PO3 4 at depth. This suggest that there is a process consuming PO3 4

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Nitrate (µ µM) 20

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Nitrate (µM) 60

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Nitrate (µM)

80 120 160

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140 m

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Depth (cm)

Depth (cm)

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Nitrate (µM) 0

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Nitrate (µM) 60

0

0

20

40

60

5 10 10

Depth (cm)

Depth (cm)

15 20 25 30

20

30

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35 40

1200 m

50

1850 m

Fig. 5. Porewater nitrate concentrations. Note the different x-axis scales for the 300 and 940 m sites. The scattered data and high values shown for the 300, 940 and 1200 m sites may be the result of ammonium oxidation during sampling, and are excluded from the interpretation.

could be the precipitation of carbonate fluorapatite. Indeed, profiles in sediments from the Long similar porewater PO3 4 Island Sound and Mississippi Delta (Ruttenberg and Berner, 1993), and further north on the Pakistan margin (Schenau et al., 2000), have been attributed to carbonate fluorapatite precipitation. profiles that are relatively constant with Furthermore, PO3 4 depth, while NH+4 concentrations increase (Figs. 1 and 3), are removal mechanism such as carbonate suggestive of a PO3 4 fluorapatite formation (Ruttenberg and Berner, 1993; Schenau et al., 2000). Thus, the precipitation of solid phosphates may well be occurring on the Pakistan margin at depths in the sediment greater than those sampled here, although this could be seen as that were frequently being at odds with the effluxes of PO3 4 observed. Cross-margin oxygen gradients also influenced the patterns of  sedimentary nitrogen cycling. Surface NO 2 and NO3 concentra-

tions and sediment penetration increased from the shallow and OMZ sites (the 140, 300 and 940 m sites) to the 1200 and 1850 m sites. Denitrification studies suggest that NO 3 is consumed at a greater rate in the sediments (and possibly in the bottom water) at the 140 and 300 m sites compared to the deeper sites (Schwartz et al., 2009). This is consistent with the interdependent low oxygen availability and high organic matter availability at these  sites, and explains the between-site variation in NO 2 and NO3 profiles. Also, oxygen availability at the 1850 m site indicates that denitrification was probably a sufficiently minor process to allow a flux of NO 3 out of the sediment as a result of nitrification (Fig. 8). Considering the range of measured NO 3 influxes at the 140, 300, 940 and 1200 m sites, and the area of seafloor impacted by the Arabian Sea oxygen minimum zone (285,000 km2, Helly and Levin, 2004); Arabian Sea sediments are estimated to consume between 1.4 and 7.9 Tg N a1 (average 2.5 Tg N a1). Water-column

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µM) Phosphate (µ 50

Silicate (µM)

100 150

-0.5

0

Ammonia (µM) 200

-0.5

1

2.5

2.5

2.5

4

4

4

5.5

7

Depth (cm)

1

5.5

7

8.5

10

10

10

11.5

11.5

11.5

13

13

13

-0.5

-0.5

2.5

2.5

4

4 Depth (cm)

1

7

6

12

7 8.5

10

10

13

0

5.5

8.5

11.5

200

Nitrite (µM)

50 100 150

1

5.5

100

7

8.5

0

0

5.5

8.5

Nitrate (µM)

Depth (cm)

100

1

Depth (cm)

Depth (cm)

-0.5

0

341

11.5 13

Fig. 6. Replicate nutrient profiles from five cores collected at a depth of 700 m on the Pakistan margin during cruise CD 150. Dotted lines show the profiles from three cores collected from one coring drop, while dashed and solid lines show profiles from two cores collected on a separate coring drop (T. Shimmield, pers. comm.).

denitrification in the Arabian Sea, which accounts for up to 30% of global marine denitrification (Cowie, 2005), is estimated at 10–44 Tg N a1 (Devol et al., 2006, and references therein). Thus, it appears that sedimentary NO 3 consumption may either contribute a substantial amount, or add a substantial amount, to the water-column total. Therefore, NO 3 consumption by Arabian

Sea sediments is likely to play a significant role in determining ocean nutrient budgets, especially in light of recent suggestions that surface ocean nitrogen fixation is largely driven by the production of nitrate-poor water in OMZs (Deutsch et al., 2007). A relative lack of denitrification allowed the 1850 m site to display a sub-surface NH+4 minimum, consistent with the

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Silicate

0.08

0.3

0.06

0.25 mmoles m-2 d-1

mmoles m-2 d-1

Phosphate

0.04 0.02 0

0.15 0.1 0.05 0

-0.02

-0.05 140

300

940

1200

1850

1200

1850

140

300

940

1200

1850

Ammonia

0.3 mmoles m-2 d-1

0.2

0.2 0.1 0 -0.1 -0.2 -0.3 140

300

940

Fig. 7. Nutrient benthic fluxes derived from modelling of porewater profiles. Note that positive numbers represent fluxes out of the sediment. The values are averages of all modelled fluxes produced for each nutrient at each site (see Table 2), and error bars are 71 standard deviation.

Table 3 Measured nutrient fluxes in mmoles m2 d1.

Phosphate CD 151 SF CD 151 EF CD 146 SF Silicate CD 151 SF CD 151 EF CD 146 SF Ammonia CD 151 SF CD 151 EF CD 146 SF Nitrate CD 151 SF CD 151 EF CD 146 SF Nitrite CD 151 SF CD 151 EF CD 146 SF

140

300

940

1200

1850

0.04770.004 0.038 0.02870.010

0.03270.005 0.060 0.01270.013

0.10070.003 0.100

– – 0.23570.237

0.00370.027 – 0.00470.002

0.66770.148 1.601 1.29170.359

0.61870.052 2.545

0.90770.0 1.595

– –

a

a

0.71170.141 – 0.0070.01

0.045 0.359 0.01170.015

0.03670.030 0.018 0.18370.004

0.02470.029 0.335

0.63470.010 0.000 0.09370.007

0.37070.032 2.193 5.40770.214

0.01370.046 0.000 0.00770.010

0.12670.018 0.130 0.48970.004

a

0.86370.046 – –

a

0.06270.088 – 0.04070.009

3.06770.564 0.423

– –

a

a

0.15070.039 0.007

– –

a

a

0.21270.009 0.11670.164 – 0.370.7 0.06170.173 – 0.1170.06

SF indicates shipboard nutrient flux measurements and EF indicates benthic lander flux measurements. For shipboard incubations the values are averages of measurements taken from two replicate cores, and the errors are 7 the variance between two replicates. The symbol ‘–’ indicates no such experiment conducted. a Data missing due to insufficient sample volume, sample loss or analytical error.

occurrence of nitrification, and anoxic oxidation of NH+4 by  NO 2 , NO3 (the anammox reaction) and/or MnO2 (Luther et al., 1997; Rysgaard et al., 2004; Thamdrup et al., 2006). The findings of Schwartz et al. (2009) also support the occurrence of anammox at the 1850 m site. Anammox may be occurring at other sites, but its effect on porewater profiles is masked by denitrification.

Cross-margin patterns in silicate concentrations however did not seem to be related to oxygen concentration. The observed increase in down-core silicate concentrations with increasing water depth is consistent with previous observations on the Goban spur, where it was attributed to increased biogenic silica dissolution (Lohse et al., 1998). The 140 m site on the Pakistan margin showed sub-surface silicate peaks, at 2 cm depth, which

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Modelled

Phosphate

0.05

3 2.5 mmoles m-2 d-1

mmoles m-2 d-1

Silicate

146 SF 151 SF EF

0.1

343

0 -0.05 -0.1

2 1.5 1 0.5 0 -0.5 -1

-0.15

-1.5 140

300

940

1200

1850

140

Ammonia

1

940

1200

1850

300

940

1200

1850

Nitrate

0

0.3

mmoles m-2 d-1

mmoles m-2 d-1

0.5

300

0.1 -0.1 -0.3

-1 -2 -3 -4 -5

-0.5

-6 140

300

940

1200

1850

300

940

1200

1850

140

Nitrite 0.7 mmoles m-2 d-1

0.6 0.5 0.4 0.3 0.2 0.1 0.0 -0.1 -0.2 140

Fig. 8. Modelled and measured benthic nutrient fluxes. Positive values indicate fluxes out of the sediment. 146 SF ¼ inter-monsoon shipboard flux measurements; 151SF ¼ post-monsoon shipboard flux measurements; EF ¼ benthic lander flux measurements. Modelled fluxes are the averages of results of modelling several separate cores (see Table 2), and error bars are 71 standard deviation. Where error bars are present on measured fluxes, the flux is the average of the two replicate cores used in each + shipboard measurement, and the error bars are 7the variance. The shipboard measured fluxes of PO3 4 and NH4 into the sediment (at the 140, 300 and 940 m sites), and the large measured efflux of NO 2 at the 300 m site are thought to be anomalies caused by oxygen contamination.

may be due to aluminosilicate precipitation at depth (Zabel et al., 1998).

4.3. Seasonal variations A monsoon-driven pulse of organic matter to the sediment may be expected to cause increased porewater nutrient concentrations, increased fluxes of most nutrients out of the sediment, and increased denitrification and nitrate drawdown. However, apart from the oxygen-driven alteration of PO3 4 profiles at the 140 m site in the post-monsoon season, no clear, systematic seasonal changes in porewater profiles or nutrient fluxes occurred (Figs. 1–5). This lack of obvious seasonal change in nutrient fluxes is consistent with observations at some abyssal sites (3200–4400 m) in the Arabian Sea (Grandel et al., 2000). In Massachusetts and Cape Cod Bays (water depth 17–76 m), maximal fluxes were observed after the spring bloom (Hopkinson et al., 2001). By inference, therefore, the lack of clear seasonal variability in nutrient concentrations and fluxes on the Pakistan margin might be attributed to a relative lack of seasonal organic matter pulse to

the seafloor. This is generally supported by a lack of clear increase in bulk organic C content or pigment and carbohydrate abundances in surface sediments after the monsoon (Cowie et al., 2009; Woulds and Cowie, 2009). However, it is a surprising result given the strong seasonal changes in upwelling and productivity that are typical of the region, and may be at odds with observations of increased sediment lipid concentrations (Jeffreys et al., 2009), an extended OMZ, shallower sediment O2 penetration and increased directly measured denitrification rates after the monsoon Brand and Griffiths, 2009; Breuer et al., 2009; Schwartz et al., 2009). It is therefore possible that porewater nutrient profiles are ‘‘buffered’’, time-averaged features that do not alter on seasonal timescales.

4.4. Comparison with other regions The following section compares our nutrient data to those from previous studies carried out at sites representing a range of depths and conditions, in order to put the Pakistan margin into context within the global ocean.

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Table 4 Previously published nutrient fluxes for a range of marine settings. Depth (m)

Eastern South Atlantic Central Equatorial N Pacific Porcupine Abyssal Plain Abyssal Arabian Sea Somali Margin Goban Spur Eastern North Pacific Washington Margin Chilean Margin Massachusetts/Cape Cod Bay Seine Estuary

1000–5700 4500–5000 44800 3188–4424 500–4000 208–4468 400–900 42–630 27–88 17–76 Intertidal

Fluxes in mmoles m2 d1 Phosphate

Silicate

0–0.03

0–0.002 0.3–0.4

Ammonia

0.007 0.01–0.04 0.007–0.011 0–0.086

0–0.2 0.3–0.8

0.2–0.9 0.2–2.3 0.25–1.1 0.3–3.4 1.9–14.3

3.6–6.7

Source

Modelled Measured Measured Modelled Modelled Measured Modelled Measured NH+4 measured, NO 3 modelled Measured Modelled

Hensen et al. (1998) Berelson et al. (1990) Brunnegard et al. (2004) Grandel et al. (2000) Koning et al. (1997) Lohse et al. (1998) Berelson et al. (2005) Devol and Christensen (1993) Munoz et al. (2004)

Nitrate 0.027–0.493 0.027–0.033 0.052

0.02–0.12

0.016–0.245

0–0.79 0.55–2.18

0.78 to 2.4 0.027 to 0.17

0.3–1.7 0.1–0.3

Method

0.1–0.3

Hopkinson et al. (2001) Bally et al., 2004

Positive numbers indicate fluxes out of the sediment. Where ranges are given for both depth and fluxes, the larger fluxes are usually associated with the shallower depths.

4.4.1. Porewater nutrient profiles At abyssal sites (3200–4400 m depth) in the Arabian Sea, Grandel et al. (2000) reported phosphate and silicate profiles and concentrations generally similar to those reported here. However,  NO 2 +NO3 concentrations were greater at the abyssal Arabian Sea sites than on the Pakistan margin, with surface concentrations of 40 mM, and penetrations of up to 25 cm. In contrast, NH+4 concentrations were comparatively low (usually below 20 mM). These differences are consistent with the increased oxygen concentrations, reduced organic matter concentrations and reduced occurrence of denitrification at the abyssal sites. Sediments from the central equatorial north Pacific (4500–5000 m depth, Berelson et al., 1990), the Goban Spur (200–4500 m depth, Lohse et al., 1998), and the Porcupine Abyssal Plain (44800 m depth, Brunnegard et al., 2004) (Table 4) show similar relationships to the Pakistan  margin, having similar PO3 4 and H4SiO4 concentrations, higher NO2  + and NO3 concentrations, and lower NH4 concentrations. Silicate concentrations in sediments from the Somali, Oman, Mexican and Californian margins are reported to be much higher (100–600 mM) than those on the Pakistan margin (Table 4) (Koning et al., 1997; Passier et al., 1997; Berelson et al., 2005). Surface ocean productivity and sediment organic carbon concentrations are higher on the west side of the Arabian Sea than on the east (Pedersen et al., 1992; Haake et al., 1993; Cowie et al., 1999). This may imply a difference in biogenic opal input, and thus explain the difference in porewater H4SiO4 concentrations between the Pakistan margin and the Oman and Somali margins. and H4SiO4 concentrations were Thus, Pakistan margin PO3 4 comparable to relatively organic matter-poor abyssal sites. The and NO concentrations and increased NH+4 reduced NO 2 3 concentrations compared to other deep-sea sites are consistent with the presence of the OMZ. 4.4.2. Nutrient fluxes The most striking difference between Pakistan margin sediments and those in other regions is that they were a sink of  NO 3 and NO2 rather than a source (Hensen et al., 1998; Lohse et al., 1998; Hopkinson et al., 2001; Brunnegard et al., 2004). This is apparently due to hypoxic conditions and intense sedimentary denitrification, especially at the 140, 300 and 940 m sites. Fluxes of NO 3 into the sediment have also been observed on the Washington margin, Mexican margin, and off central Chile (Table 4; Devol and Cristensen, 1993; Hartnett and Devol, 2003; Munoz et al., 2004), where bottom-water hypoxia also occurs. (modelled and measured) on the Benthic fluxes of PO3 4 Pakistan margin were generally similar to previously reported

values from abyssal settings such as the abyssal Arabian Sea (Grandel et al., 2000), the Goban Spur (Lohse et al., 1998) and the eastern South Atlantic (Hensen et al., 1998). Silicate fluxes were similar to those reported from the same regions, plus the central equatorial north Pacific (Berelson et al., 1990), and the Somali margin of the Arabian Sea (Koning et al., 1997) (Table 4). Ammonium fluxes were similar to those seen at shallower sites on the Chilean and Washington margins (Devol and Cristensen, 1993; Munoz et al., 2004), and in Massachusetts and Cape Cod Bays (Hopkinson et al., 2001). Thus, fluxes of PO3 4 and H4SiO4, on the Pakistan margin were more consistently similar to deeper (margin and abyssal) sites, NH+4 fluxes were generally more similar to those previously measured at shallower sites, and NO 3 fluxes were only comparable to those previously reported from hypoxic regions.

4.5. Flux estimation methods In light of the challenges associated with measuring the fluxes of redox-sensitive nutrients at sites which often displayed extremely low bottom-water oxygen concentrations and complex biogeochemical regimes, it is perhaps unsurprising that measured and modelled nutrient fluxes in this study did not always match (Fig. 7), either in magnitude or direction. Several previous studies have compared modelling of porewater nutrient profiles and direct measurement as methods for quantifying benthic nutrient fluxes. Berelson et al. (1990) found that the two methods agreed within 40–50% for abyssal sites in the central equatorial north Pacific, while at continental margin sites, measured fluxes have been found to exceed modelled fluxes by factors of 4–29 (Devol and Cristensen, 1993; Rasheed et al., 2006). Where there was agreement of direction between modelled and some of the measured fluxes on the Pakistan margin, (Fig. 8) the measured fluxes were greater by a factor of 1–31. These factors are similar to the range of factors found in most previous continental margin studies. However, Lohse et al. (1998) found that measured H4SiO4 fluxes agreed with modelled fluxes within error. The differences between methods have be attributed to advective porewater exchange during bioturbation, which is often not accounted for during modelling (and that is true of the modelling in this study), and to the difficulty of accurately characterising the benthic boundary layer (Koning et al., 1997). Both of these factors are likely to contribute to differences between modelled and measured fluxes on the Pakistan margin.

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5. Conclusions

 Bottom-water dissolved oxygen concentrations were found to

 





exert a strong influence over nutrient concentrations and fluxes through redox-dependent processes such as denitrification and sorption of PO3 4 . Nitrate drawdown, most probably linked to denitrification, appeared particularly important, and may cause Arabian Sea sediments to be an NO 3 sink of global significance. Nutrient profiles and fluxes were not significantly influenced by the summer monsoon and any associated OM pulse to the sediment, but PO3 4 profiles at the 140 m site were affected by a seasonal expansion of the OMZ. Phosphate and H4SiO4 concentrations and fluxes were found to be similar to those reported for other deep-sea sites, while NH+4 and NO 3 concentrations and fluxes were consistent with those seen at other productive, hypoxic margin sites. Modelling of porewater profiles quite consistently produced calculated fluxes that were less than measured values, suggesting that processes in the benthic boundary layer, and the influence of bioturbation-induced advective porewater exchange are important processes on the Pakistan margin. Shipboard flux determinations were complicated by potential oxygen contamination problems, and differences between in situ and shipboard measurements highlighted the difficulties inherent in attempts to maintain low ambient oxygen concentrations during shipboard incubation studies.

Acknowledgements The authors would like to thank Eric Breuer, Sue McKinley and Terrie Sawyer for help with core collection and sectioning; Tasos Anestis, who together with Tim Brand and Steve Mowbray conducted the shipboard nutrient analyses; and Oli Peppe and Willie Thompson who ran the benthic lander. We would also like to thank two anonymous reviewers, whose comments helped us to improve the manuscript. This work was conducted aboard the RRS Charles Darwin, and was made possible by grants from the Natural Environmental Research Council of the UK and the Leverhulme Trust. References Bally, G., Mesnage, V., Deloffre, J., Clarisse, O., Lafite, R., Dupont, J.-P., 2004. Chemical characterization of porewaters in an intertidal mudflat of the Seine estuary: relationship to erosion-deposition cycles. Marine Pollution Bulletin 49, 163–173. Berelson, W.M., Hammond, D.E., O’Neil, D., Xu, X.-M., Chin, C., Zukin, J., 1990. Benthic fluxes and pore water studies from sediments on the central equatorial north Pacific: nutrient diagenesis. Geochemica et Cosmochemica Acta 54, 3001–3012. Berelson, W.M., Prokopenko, M., Sasone, F.J., Graham, A.W., McManus, J., Bernhard, J.M., 2005. Anaerobic diagenesis of silica and carbon in continental margin sediments: discrete zones of TCO2 production. Geochemica et Cosmochemica Acta 69, 4611–4629. Berg, P., Risgaard-Petersen, N., Rysgaard, S., 1998. Interpretation of measured concentration profiles in sediment pore water. Limnology and Oceanography 43, 1500–1510. Black, K.S., Fones, G.R., Peppe, O.C., Kennedy, H.A., Bentaleb, I., 2001. An autonomous benthic lander: preliminary observations from the UK BENBO thematic programme. Continental Shelf Research 21, 859–877. Brand, T., Griffiths, C., 2009. Seasonality in the hydrography and biogeochemistry across the Pakistan margin of the NE Arabian Sea. Deep Sea Research II 56, 283–295. Breuer, E.R., Law, G.T.W., Woulds, C., Cowie, G.L., Shimmield, G.B., Peppe, O., Schwart, M., McKinlay, S., 2009. Sedimentary oxygen consumption and microdistribution at sites across the Arabian sea oxygen minimum zone (Pakistan margin). Deep-Sea Research II 56, 296–304. Brunnegard, J., Grandel, S., Stahl, H., Tengberg, A., Hall, P.O.J., 2004. Nitrogen cycling in deep-sea sediments of the Porcupine Abyssal Plain, NE Atlantic. Progress in Oceanography 63, 159–181.

345

Cowie, G.L., 2005. The biogeochemistry of Arabian Sea surficial sediments: a review of recent studies. Progress in Oceanography 65, 260–289. Cowie, G.L., Mowbray, S., Lewis, M., Matheson, H., McKenzie, R., 2009. Carbon and nitrogen stable isotopic compositions of surficial sediments from the Pakistan margin of the Arabian Sea. Deep Sea Research II 56, 271–280. Cowie, G.L., Calvert, S.E., Pedersen, T.F., Schulz, H., Von Rad, U., 1999. Organic content and preservational controls in surficial shelf and slope sediments from the Arabian Sea (Pakistan margin). Marine Geology 161, 23–38. De Maison, G.J., Moore, G.T., 1980. Anoxic environments and oil source bed genesis. American Association of Petroleum Geologists Bulletin 64 (8), 1179–1209. Deutsch, J.L., Sarmiento, J.L., Sigman, D.M., Gruber, N., Dunne, J.P., 2007. Spatial coupling of nitrogen inputs and losses in the ocean. Nature 445, 163–167. Devol, A.H., Cristensen, J.P., 1993. Benthic fluxes and nitrogen cycling in sediments of the continental margin of the eastern North Pacific. Journal of Marine Research 51, 345–372. Devol, A.H., Uhlenhopp, A.G., Naqvi, S.W.A., Brandes, J.A., Jayakumar, D.A., Naik, H., Gaurin, S., Codispoti, L.A., Yoshinari, T., 2006. Denitrification rates and excess nitrogen gas concentrations in the Arabian Sea oxygen deficient zone. Deep Sea Research I 53, 1533–1547. Ganeshram, R.S., Pedersen, T.F., Calvert, S.E., Murray, J.W., 1995. Large changes in oceanic nutrient inventories from glacial to interglacial periods. Nature 376 (6543), 755–758. Ganeshram, R.S., Pedersen, T.F., Calvert, S.E., McNeill, G.W., Fontugne, M.R., 2000. Glacial–interglacial variability in denitrification in the world’s oceans: causes and consequences. Paleoceanography 15 (4), 361–376. Glud, R.N., Gundersen, J.K., Revsbech, N.P., Jorgensen, B.B., Huettel, M., 1995. Calibration and performance of the stirred flux chamber from the benthic lander Elinor. Deep Sea Research I 42, 1029–1042. Gooday, A.J., Levin, L.A., Aranda da Silva, A., Bett, B.J., Cowie, G.L., Gage, J.D., Hughes, D.J., Jeffreys, R.M., Lamont, P.A., Larkin, K.E., Murty, S.J., Schumacher, S., Whitcraft, C., Woulds, C., 2009. Faunal responses to oxygen gradients on the Pakistan margin: a comparison of foraminifera, macrofauna and megafauna. Deep Sea Research II 56, 488–502. Grandel, S., Rickert, D., Schluter, M., Wallmann, K., 2000. Pore-water distribution and quantification of diffusive benthic fluxes of silicic acid, nitrate and phosphate in surface sediments of the deep Arabian Sea. Deep Sea Research II 47, 2707–2734. Haake, B., Ittekkot, V., Rixen, T., Ramaswamy, V., Nair, R.R., Curry, W.B., 1993. Seasonality and interannual variability of particle fluxes to the deep Arabian Sea. Deep Sea Research Part I 40 (7), 1323–1344. Hartnett, H.E., Devol, A.H., 2003. Role of a strong oxygen-deficient zone in the preservation and degradation of organic matter: a carbon budget for the continental margins of morthwest Mexico and Washington State. Geochemica et Cosmochemica Acta 67 (2), 247–264. Helly, J.J., Levin, L.A., 2004. Global distribution of naturally occurring marine hypoxia on continental margins. Deep Sea Research Part I 51, 1159–1168. Hensen, C., Landenberger, H., Zabel, M., Schulz, H.D., 1998. Quantification of diffusive benthic fluxes of nitrate, phosphate, and silicate in the southern Atalntic Ocean. Global Biogeochemical Cycles 12, 193–210. Hopkinson Jr., C.S., Giblin, A.E., Tucker, J., 2001. Benthic metabolism and nutrient regeneration on the continental shelf of Eastern Massachusetts, USA. Marine Ecology Progress Series 224, 1–19. Hughes, D.J., Lamont, P.A., Levin, L.A., Packer, M., Gage, J.D., 2009. Macrofaunal community and sediment structure across the Pakistan margin Oxygen Minimum Zone, North-East Arabian Sea. Deep-Sea Research II 56, 434–448. Jahnke, R., Richards, M., Nelson, J., Robertson, C., Rao, A., Jahnke, D., 2005. Organic matter remineralization and porewater exchange rates in permeable South Atlantic Bight continental shelf sediments. Continental Shelf Research 25, 1433–1452. Jeffreys, R.M., Wolff, G.A., Cowie, G.L., 2009. Influence of oxygen on heterotrophic reworking of sedimentary lipids at the Pakistan margin. Deep Sea Research II 56, 358–375. Koning, E., Brummer, G.-J., Van Raaphorst, W., Van Bennekom, J., Helder, W., Van Iperen, J., 1997. Settling, dissolution and burial of biogenic silica in the sediments off Somalia (northwestern Indian Ocean). Deep Sea Research II 44, 1341–1360. Larkin, K.E., Gooday, A.J., 2009. Foraminiferal faunal responses to monsoon-driven changes in organic matter and oxygen availability at 140 and 300 m water depth in the NE Arabian Sea. Deep Sea Research II 56, 403–421. Law, G., Shimmield, T.M., Shimmield, G.B., Cowie, G.L., Breuer, E.R., Harvey, S.M., 2009. Manganese, iron and sulphur cyclling on the Pakistan margin. Deep Sea Research II 56, 305–323. Levin, L.A., Whitcraft, C., Mendoza, G.F., Gonzalez, J.P., Cowie, G.L., 2009. Oxygen and organic matter thresholds for benthic faunal activity on the Pakistan margin oxygen minimum zone (700–1100 m). Deep-Sea Research II 56, 449–471. Li, Y.H., Gregory, S., 1974. Diffusion of ions in seawater and in deep-sea sediments. Geochemica et Cosmochemica Acta 38 (5), 703–714. Lohse, L., Helder, W., Epping, E.H.G., Balzer, W., 1998. Recycling of organic matter along a shelf-slope transect across the N.W. European Continental Margin (Goban Spur). Progress in Oceanography 42, 77–110. Luther, G.W., Sundby, B., Lewis, B.L., Brendel, P.J., Silverberg, N., 1997. Interactions of manganese with the nitrogen cycle: alternative pathways to dinitrogen. Geochimica et Cosmochimica Acta 61 (19), 4043–4052.

ARTICLE IN PRESS 346

C. Woulds et al. / Deep-Sea Research II 56 (2009) 333–346

Munoz, P., Salamanca, M.A., Neira, C., Sellanes, J., 2004. Nitrogen sediment fluxes in an upwelling system off central Chile (Concepcion Bay and adjacent shelf) during the 1997–1998 El Nino. Revista Chilena de Historia Natural 77, 305–318. Passier, H.F., Luther, G.W., De Lange, G.J., 1997. Early diagenesis and sulphur speciation in sediments of the Oman Margin, northwestern Arabian Sea. Deep Sea Research II 44, 1361–1380. Pedersen, T.F., Shimmield, G.B., Price, N.B., 1992. Lack of enhanced preservation of organic matter in sediments under the oxygen minimum zone on the Oman Margin. Geochemica et Cosmochemica Acta 56, 545–551. Rasheed, M., Al-Rousan, S., Manasrah, R., Al-Horani, F., 2006. Nutrient fluxes from deep sediment support nutrient budget in the oligitrophic waters of the Gulf of Aqaba. Journal of Oceanography 62, 83–89. Ruttenberg, K.C., Berner, R.A., 1993. Authigenic apatite formation and burial in sediments from non-upwelling, continental margin environments. Geochemica et Cosmochemica Acta 57, 991–1007. Rysgaard, S., Glud, R.N., Risgaard-Petersen, N., Dalsgaard, T., 2004. Denitrification and anammox activity in Arctic marine sediments. Limnology and Oceanography 49, 1493–1502.

Schenau, S.J., Slomp, C.P., De Lange, G.J., 2000. Phosphogenesis and active phosphorite formation in sediments from the Arabian Sea oxygen minimum zone. Marine Geology 169, 1–20. Schulz, H.D., Zabel, M., 2006. Marine Geochemistry. Springer, Berlin. Schwartz, M.C., Woulds, C., Cowie, G.L., 2009. Sedimentary denitrification rates across the Arabian Sea oxygen minimum zone. Deep Sea Research 56, 324–332. Thamdrup, B., Dalsgaard, T., Jensen, M.M., Ulloa, O., Farias, L., Escribano, R., 2006. Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnology and Oceanography 51, 2145–2156. van Raaphorst, W., Kloosterhuis, H.T., 1994. Phosphate sorption in superficial intertidal sediments. Marine Chemistry 48 (1), 1–16. Woulds, C., Cowie, G.L., 2009. Sedimentary pigments on the Pakistan margin: controlling factors and organic matter dynamics. Deep Sea Research II 56, 347–357. Zabel, M., Dahmke, A., Schulz, H.D., 1998. Regional distribution of diffusive phosphate and silicate fluxes through the sediment–water interface: the eastern South Atlantic. Deep Sea Research I 45, 277–300.