oxygen minimum zones (omzs) in the modern ocean
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Progress in Oceanography 80 (2009) 113–128
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Progress in Oceanography
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Oxygen minimum zones (OMZs) in the modern ocean
A. Paulmier a,b,*, D. Ruiz-Pino b
a LEGOS/CNRS 18, Av. Ed. Belin, 31401 Toulouse Cedex 9, Franceb LOCEAN, Université P&M Curie, Courrier 134, 4 pl. Jussieu, 75252 Paris Cedex 05, France
a r t i c l e i n f o
Article history:Received 6 September 2007Received in revised form 1 August 2008Accepted 4 August 2008Available online 17 August 2008
Keywords:Oxygen minimum zones (OMZs)OxygenGlobal oceanDenitrificationBiogeochemistry
0079-6611/$ - see front matter � 2008 Elsevier Ltd. Adoi:10.1016/j.pocean.2008.08.001
* Corresponding author. Address: LEGOS/CNRS 18, ACedex 9, France. Tel.: +33 (0)561333007; fax: +33 (0)
E-mail address: [email protected]
a b s t r a c t
In the modern ocean, oxygen minimum zones (OMZs) are potential traces of a primitive ocean inwhich Archean bacteria lived and reduced chemical anomalies occurred. But OMZs are also keys tounderstanding the present unbalanced nitrogen cycle and the oceans’ role on atmospheric greenhousecontrol. OMZs are the main areas of nitrogen loss (as N2, N2O) to the atmosphere through denitrifi-cation and anammox, and could even indirectly mitigate the oceanic biological sequestration ofCO2. It was recently hypothesized that OMZs are going to spread in the coming decades as a conse-quence of global climate change. Despite an important OMZ role for the origin of marine life and forthe biogeochemical cycles of carbon and nitrogen, there are some key questions on the structure ofOMZs at a global scale. There is no agreement concerning the threshold in oxygen that defines anOMZ, and the extent of an OMZ is often evaluated by denitrification criteria which, at the same time,are O2-dependent.
Our work deals with the identification of each OMZ, the evaluation of its extent, volume and ver-tical structure, the determination of its seasonality or permanence and the comparison between OMZsand denitrification zones at a global scale. The co-existence in the OMZ of oxic (in its boundaries) andsuboxic (even anoxic, in its core) conditions involves rather complex biogeochemical processes suchas strong remineralization of the organic matter, removal of nitrate and release of nitrite. The quan-titative OMZ analysis is focused on taking into account the whole water volume under the influenceof an OMZ and adapted to the study of the specific low oxygen biogeochemical processes.
A characterization of the entire structure for the main and most intense OMZs (O2 < 20 lM reaching1 lM in the core) is proposed based on a previously published CRIO criterion from the eastern SouthPacific OMZ and including a large range of O2 concentrations. Using the updated global WOA2005 O2
climatology, the four known tropical OMZs in the open ocean have been described: the Eastern SouthPacific and Eastern Tropical North Pacific, in the Pacific Ocean; the Arabian Sea and Bay of Bengal, inthe Indian Ocean. Moreover, the Eastern Sub-Tropical North Pacific (25–52�N) has been identified asa lesser known permanent deep OMZ. Two additional seasonal OMZs at high latitude have also beenidentified: the West Bering Sea and the Gulf of Alaska. The total surface of the permanent OMZs is30.4 millions of km2 (�8% of the total oceanic area), and the volume of the OMZ cores (10.3 millionsof km3) corresponds to a value �7 times higher than previous evaluations. The volume of the OMZcores is about three times larger than that of the associated denitrification zone, here defined asNMZ (‘nitrate deficit or NDEF > 10 lM’ maximum zone). The larger OMZ, relative to the extent of deni-trification zone, suggests that the unbalanced nitrogen cycle on the global scale could be more intensethan previously recognized and that evaluation of the OMZ from denitrification could underestimatetheir extent.
� 2008 Elsevier Ltd. All rights reserved.
1. Introduction
The interest in oxygen minimum zones (OMZs), characterizedherein as O2-deficient layers in the ocean water column, is quite re-cent, since the appearance of the name ‘‘OMZ” in Cline and Richards
ll rights reserved.
v. Ed. Belin, 31401 Toulouse561253205.r (D. Ruiz-Pino).
(1972). OMZs correspond to subsurface oceanic zones (e.g., at 50–100 m depth in the Arabian Sea; Morrison et al., 1999) and reachingultra-low values of O2 concentration (e.g. <1 lM; Karstensen et al.,2008). OMZs, because of their intensity and shallowness, are, a priori,different from the relatively well known ‘‘classical O2 minimum”,which is �50 times more oxygenated than OMZs and found atintermediate depths (1000–1500 m) in all the oceans (Wyrtki,1962). Note that in the present study, an OMZ is defined as being‘‘more intense’’, when the O2 concentrations in its core are lower.
114 A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128
1.1. OMZ specificities for marine biogeochemistry and ecosystems
OMZs have been mainly known for playing an essential role inthe global nitrogen cycle, in which various chemical species,according to their degree of oxidation (e.g. ammonium, NHþ4 ;nitrite, NO�2 ; nitrate, NO�3 ; nitrous oxide, N2O; dinitrogen, N2),and different bacterial processes intervene. Under oxic conditions,but also at the upper boundary (oxycline) of an OMZ, nitrificationtransforms NHþ4 into NO�3 . But OMZs are especially associated withdenitrification, which is a bacterial process occurring only inO2-deficient regions (e.g., Codispoti et al., 2001). Denitrificationconverts NO�3 , one of the main limiting nutrients in the ocean, intogaseous nitrogen (N as, for example, N2O, N2) which is lost to theatmosphere and contributes to the oceanic nitrate deficit (N/P � 14.7; e.g., Tyrrell, 1999). However, recently, an unknown pro-cess in the ocean has been observed, first in sediments and thenin the water column in the OMZs (e.g., Kuypers et al., 2003): theanaerobic oxidation of NHþ4 using NO�2 (anammox); this imposesa complete revision of the global nitrogen cycle (e.g., Arrigo,2005). OMZs are also involved in the cycle of very important cli-matic gases: (i) production of �50% of the oceanic N2O (e.g., Bangeet al., 1996); (ii) production of H2 S (e.g., Dugdale et al., 1977) andCH4 (e.g., Cicerone and Oremland, 1988), episodically or for OMZsin contact with sediments; (iii) limitation of atmospheric CO2
sequestration by the ocean: directly as an end-product of reminer-alization (Paulmier et al., 2006) or indirectly through limitation oftotal primary production due to the N loss (see hypothesis of Fal-kowski, 1997); (iv) potential DMS consumption due to higher bac-terial activity (Kiene and Bates, 1990). Chemically, OMZs areassociated with acidification (low pH � 7.5 SWS; Paulmier, 2005),and reduced conditions (Richards, 1965) favoring reduced chemi-cal species (e.g., Fe(II) or Cu(I) potentially stimulating photosynthe-sis or N2O production).
OMZs have also increased interest in biological and ecosystemstudies. Because of similarities between Archean bacteria and thoseliving in the OMZs (Zumft, 1997), OMZs could be considered as ana-logues of the primitive anoxic ocean in which life is widely thoughtto have first appeared. Transitions from high to low (the appearanceof OMZs) oxygenation periods could stimulate biodiversity on apaleoclimatic scale (Rogers, 2000). OMZs can be a refuge for organ-isms specifically adapted to low O2 concentration (e.g., giant Thiop-loca bacteria; Levin, 2002) from predation or competition withother species, and the lower OMZ boundary can even be amongthe richest habitats for the megafauna of the ocean. As a respiratorybarrier, OMZs are associated with active vertical daily migration(e.g., for zooplankton; Fernández-Alamo and Färber-Lorda, 2006).But, for the main species (e.g., commercial fishes, such as anchovy),OMZs are considered as inhospitable. In the past, the Oceanic An-oxic Events (OAEs) have been associated with massive speciesextinction (e.g. during the Mid-Cretaceous). In the present, episodicanoxic events associated with eutrophicated waters are also induc-ing massive abnormal fish mortality (e.g., Chan et al., 2008).
1.2. Need for a reference state and an O2 criterion for defining theOMZs extent
The intensity of all OMZ’s perturbations and their potentialfeedback to climate and the marine ecosystem would depend onthe OMZs extent. This extent would vary in response to climaticchanges (lower ventilation due to stratification, and decreased O2
solubility) and natural or anthropogenic fertilization (increasedremineralization) through nutrient or metal inputs by upwelling,river discharge or atmospheric dust fall-out (e.g., Béthoux, 1989;Joos et al., 2003). In the past, OMZs have probably extended andcontracted in warm (interglacial) and cold (glacial) periods, respec-tively (e.g., Cannariato and Kennett, 1999). Under present-day
conditions, OMZs would increase or intensify, according to obser-vations in recent decades (e.g., Stramma et al., 2008). But evalua-tions or predictions of OMZs variation over paleoclimatic periods,since the anthropocene era or in the future, cannot be validatedwithout a reference state, and the report of all the existing OMZsdetected in the modern ocean taking into account improvementsin O2-measurement techniques.
Despite the important role of OMZs in understanding primitivemarine life and chemistry, as well as in the carbon (C) and nitrogen(N) cycles, little knowledge has been obtained on the extent andvertical structure of these oceanic ‘‘curiosities”. This is mainlydue to the following difficulties: (i) few available O2 data obtainedwith a low enough detection limit (<1 lM) and accuracy (<2 lM),owing to the present limitations in the sampling and analysis tech-niques linked to the low O2 concentration; (ii) the choice of aunique criterion for all OMZs, since the nature of this criterionoften depends on research interest (e.g., specific low-O2 biogeo-chemistry process studies have to take into account an O2 concen-tration lower than 20 lM, but the influence of physical processesdo not make it necessary to include suboxic and anoxic condi-tions); (iii) the criteria could be different for each OMZ region:for example, the OMZs in the Northeastern Atlantic ocean is ex-cluded when a threshold of 20 lM is used (Helly and Levin,2004). Different terms and thresholds have been used to describedthe overall low O2 conditions. Suboxia has been mainly defined bybiologists and biogeochemists as a transition layer from O2- toNO�3 -respiration, with thresholds between �0.7 lM (e.g., Yakusevand Neretin, 1997) and 20 lM (e.g., Helly and Levin, 2004). Hypox-ia implies O2 conditions under which macro-organisms cannot live:�8 lM for Kamykowski and Zentara (1990), but up to 40 lMdepending on the species considered, such as anchovy (e.g., Grayet al., 2002). Dysoxia (O2 < 4 lM) and microxia (O2 < 1 lM; Levin,2002) are associated with a sharp O2 transition for the large organ-isms, such as fishes. Anoxia (O2 < 0.1 lM; Oguz et al., 2000) is definedby transition from NO3-respiration to sulphate-reduction.
The first global study providing information on where watercolumn OMZs can be located is that of Kamykowski and Zentara(1990) who produced maps of the distribution of hypoxia (O2 <8 lM) and of denitrification (Nitrate DEFicit or NDEF > 10 lM):ENP (Eastern North Pacific), ESP (Eastern South Pacific), AS (ArabianSea) and BB (Bay of Bengal; see Fig. 1a). Without having a knownevaluation of an OMZ’s surface and vertical structure, Codispotiet al. (2001) concluded that the volume of suboxic zones couldreach �0.1% of the oceanic volume. OMZ areas have been consid-ered to be similar to those of denitrification in several regionalstudies: ENP, ESP, AS (e.g., Codispoti et al., 2001). Hattori (1983)evaluated global oceanic denitrification (�8.45 � 106 km2),obtained from separate previous evaluations using different criteriafor each OMZ: NDEF > 10 lM (AS); secondary subsurface NO�2 peak(ESP); O2 < 5 lM (ENP). But from a qualitative comparison of hy-poxia and denitrification maps, Kamykowski and Zentara (1990)concluded that the extent of the denitrification zone would bemuch less than the extent of the OMZ. Such a difference shows thatthe denitrification criterion could not be adapted to evaluating thesize of the whole O2-deficit zone. To validate this hypothesis, it isnecessary to evaluate OMZs independently of the extent of thedenitrification zone. Note also that the surface of OMZs that is incontact with sediments (1372 � 106 km2; Helly and Levin, 2004)would be an order of magnitude lower than the global denitrifica-tion zone and the associated water-column OMZ surfaces.
Estimations of the extent of OMZs for biogeochemical studiesare scarce and/or local (e.g., Morrison et al., 1999). Recently, thequantification of OMZs in the open ocean has been proposed byKarstensen et al. (2008). In the present study, three O2 thresholdswere used (the suboxic level of 4.5 lmol/kg, a more stringent45 lmol/kg and a more relaxed level of 90 lmol/kg), and the anal-
Fig. 1. (a) O2 distribution (lM) at depth where O2 concentration is minimal, indicating the extent of the OMZs (in red) according to the WOA2005 climatology. The color barscale corresponds to a 1 ± 2 lM interval between 0 and 20 lM, and a 20 ± 2 lM interval between 20 and 340 lM. The isolines indicate the limit of the upper OMZ CORE depthin meters with a 100-m contour interval. For OMZ acronyms, see the list at the end of the main text. (b) NDEF > 10 ± 2.5 lM distribution (lM) at depth where NDEF ismaximal, indicating the extent of the NMZs from the WOA2005 climatology. The extent of the OMZs (see (a), above) is marked by contours in black.
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yses were focused on the tropical Atlantic and Pacific Oceans. TheOMZ volumes thus evaluated were of 0.461, 18.6 and 38.3 �106 km3 for each proposed O2 threshold, respectively. Althoughnot focused on the OMZs in the Indian Ocean, Karstensen et al.(2008) proposed an estimation of the vertical extent for the OMZin the Arabian Sea of 550 m, i.e. about twice as small as the local
evaluation by Morrison et al. (1999). Why another evaluation ofOMZ extent and volume? Because our focus is on defining anOMZ structure and extent which allows us to take into account spe-cific biogeochemical processes, such as denitrification or anammox,associated with low O2. The evaluation and criteria proposed byKarstensen and coauthors are more adapted to the analysis of the
116 A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128
dynamical processes responsible for the formation of an OMZ,though excluding the formation of OMZs in the Indian Ocean, whereprobably the most intense denitrification and nitrogen loss occur,and such as we will see here, do not include OMZs at a high subtrop-ical latitude. It was shown from an analysis of the ESP OMZ off Chile(Paulmier et al., 2006) that the existence of three different layershas to be taken into account to evaluate the entire OMZ structure:the oxycline (upper O2 gradient, �5 times more intense than in theoxygenated ocean); the core (O2 < 20 lM); the lower O2 gradient.Indeed, the oxycline is considered as the OMZ engine, where themost intense remineralization occurs, leading to the OMZ’s intensi-fication, and where a specific denitrification and nitrification cou-pling (e.g., Brandes et al., 2007) could also occur with O2 > 20 lM.OMZ core, specific to anaerobic processes as canonical (classicalanaerobic) denitrification, and the lower O2 gradient, where nitrifi-cation is a main process, could play an important role in the nitro-gen cycling in the OMZ (e.g., Anderson et al., 1982). Thus, toconsider the specific biogeochemical processes, it is necessary to in-clude these three layers and the large range of O2 concentrations,and not only the extremely low O2 observed in the OMZ core.Finally, having in mind to answer the question of how denitrifica-tion criteria are or are not adapted to the evaluation of the extentof an OMZ, it is necessary to determine simultaneously the struc-ture and extent of OMZ and the denitrification zones.
Hence, from the same O2 criterion and comparison with the cri-teria for denitrification, the main and most intense OMZs in theopen ocean are identified and characterized quantitatively (hori-zontally and vertically). The permanence and potential seasonalityof the OMZs will be analyzed. However, OMZs formed over thecontinental shelf (such as the Benguela OMZ) and in semi-enclosedseas (such as the Black Sea) or over deep trenches (e.g. Gulf of Car-iaco, Venezuela) reaching the level of anoxia will not be addressedin this study.
2. Methodology
To characterize and determine the surface and volume of anOMZ, the CRIO criterion on O2, adapted to take into account the en-tire vertical thickness of an OMZ, and compared with the denitrifi-cation criteria, was applied to the WOA2005 (World Ocean Atlas,2005) data.
2.1. CRIO (CRIterion on O2) criterion for OMZ estimation
The CRIO OMZ criterion is based on a characteristic O2 profiledefined for the Chilean OMZ from �200 data collected at 18 sta-tions during four cruises (2000–2002; between 20�S and 30�S),with high vertical resolution (5–10 m) sampling and an achievedaccuracy of 0.5–1.0 lM (Paulmier et al., 2006). CRIO has beendefined to take into account the OMZ core, but also the upperand lower O2 gradients, corresponding to the boundary layersbetween the core and the surrounding well oxygenated ocean, atthe top and at the bottom of the OMZ, and contributing to the Nperturbation (e.g., Anderson et al., 1982). These three OMZ layers,covering an O2 continuum from aerobic to anaerobic conditions,exhibit anomalies that differentiate them from the surroundingmore oxygenated seawater.
Since, from our biogeochemical point of view, OMZs should nec-essarily allow denitrification, an OMZ core (called CORE) has beendefined by O2 < 20 lM. Indeed, O2 < 20 lM corresponds to themaximum O2 concentration for which water-column denitrifica-tion was observed in situ (Smethie, 1987). The O2 < 20 lM concen-tration also corresponds to a usual suboxic condition used toseparate the aerobic (O2-respiration) from the denitrifying (NO�3 -respiration) activity (e.g., Oguz et al., 2000). In addition, this
threshold of 20 lM could be used with sufficient confidence, basedon the O2 detection limit and the uncertainties (�20 lM) of themain O2 databases available. Using O2 <20 lM, the CRIO criterionexcludes the OMZs (or low O2 zones called, LOZ) in the open trop-ical Atlantic Ocean (O2 > 40, and 20 lM in the Canary and BenguelaCurrent systems, respectively; Karstensen et al., 2008), in which nodenitrification has yet been reported, except on the continentalmargin (e.g., in the Benguela Current system). The present studytherefore focuses on the most intense OMZs of the open ocean,reaching the weakest concentrations (down to O2 <1 lM) in theeastern Pacific Ocean and the northern Indian Ocean. In additionto the CORE, the upper OMZ boundary layer border, called the oxy-cline (OXY), which plays a role as an OMZ biogeochemical engine(Paulmier et al., 2006), is defined by gradients higher than0.9 lM/m, as for the OMZ off Chile. The lower OMZ boundary layer,called the lower O2 gradient (LOG), is delimited by the depth atwhich the O2 gradient becomes less than 0.1 lM/m, correspondingto the strongest O2 gradient for the ‘‘classical O2 minimum”.
2.2. Denitrification criteria for NMZ (‘‘nitrate deficit” maximum zone)
Previous indirect quantifications of the vertical and horizontalextents of an OMZ used a criterion based on the denitrificationactivity, which focuses mainly on the calculation of different indi-ces (e.g., Hattori, 1983): the NO�3 deficit (NDEF > 10 lM) and/or theNO�2 secondary subsurface peak (>5 lM).
Denitrification was evaluated quantitatively with NDEF ap-proach and compared qualitatively with the subsurface NO�2 peak,which also indicates the presence of denitrification (NO�3 -reductioninto NO�2 ; Codispoti and Christensen, 1985). The ‘NDEF > 10 lM’criterion corresponding to the historical definition (NDEF ¼15PO3�
4 �NO�3 ; Broecker and Peng, 1982) and previously used atthe global scale (Kamykowski and Zentara, 1990) will be here deter-mined. N* (Gruber and Sarmiento, 1997) was not chosen, becausethe threshold corresponding to significant denitrification has notyet been well defined, absolute N* values being arbitrary (Gruber,2004), although the same conclusions as with NDEF can be obtainedwith N* < �9 lM. Thus here, from the computation of NDEF, and byanalogy with the OMZ, an NMZ (NDEF maximum zone) has beendefined corresponding to NDEF > 10 lM. In the figures, NO�2 sec-ondary subsurface peaks have been delimited arbitrarily by an iso-line corresponding to about half of the NO�2 maximum (NO�2max) tobe coherent with the NO�2max intensity of each area. This NO�2 crite-rion is in agreement with the conditions used previously for theeastern Pacific Ocean and the northern Indian Ocean (e.g., Codispotiet al., 2001).
2.3. WOA2005 database used for OMZ and NMZ estimations
CRIO and denitrification criteria were applied using WOA2005(World Ocean Atlas 2005) data obtained between 1893 and2004; this is the most recent and updated global O2 and nutrientdatabase. From WOA2005 data, including WOCE (World OceanCirculation Experiment) data and respecting WOCE quality stan-dards, a yearly climatology (Boyer et al., 2006) for O2, NO�3 andPO2�
4 global distributions was obtained and mainly used here.O2 climatology has been developed based on data from 632,888
profiles of bottle samples mainly taken in the last 30 years (>80% ofthe data; Boyer et al., 2006). The distribution of these O2 profiles is,a priori, correctly covering all the already identified hypoxic areas(ENP, ESP, AS, BB; Kamykowski and Zentara, 1990). O2 accuracyand reproducibility are <10 lM and 2–10 lM, respectively.
NO�3 and PO2�4 WOA2005 climatology’s have been used to eval-
uate NDEF and is based on the same order of profile numbers andduring the same periods as for O2, though 2.7 (233,125) and 1.6(400,399) times less abundant, respectively. Accuracy and
1 For interpretation of color in Fig. 1, the reader is referred to the web version ofthis article.
A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128 117
reproducibility are: �2 and �0.2 lM for NO�3 ; �0.03 and �0.02 lMfor PO2�
4 . No global NO�2 database is available with analytical ordata-processing errors (Kamykowski and Zentara, 1991). NO�2 hastherefore been used only for the four regions (ESP off Chile andPeru; ETNP – Eastern Tropical North Pacific; AS) for which ade-quate NO�2 data are available, from Nitrop-85 (C2–C3–C4), VERTEXI and II and Kanya cruises, respectively.
The calculation of the vertical and horizontal boundaries of theOMZ–NMZ is based on WOA2005 climatology in net common dataformat (NetCDF), corresponding to a 1 � 1 zonal and meridionalinterpolation and, temporally, to each season (Collier and Durack,2006). About three times more data are available near the coastand in the northern hemisphere than in the middle of the oceansand in the southern hemisphere, and that resolution induces an er-ror of ±10% for the horizontal extent. Vertically, a linear interpola-tion was performed between the standard depths of the O2 andthe nutrient concentrations (i.e. 10, 20, 30, 50 m, near the surface,and 1400, 1500, 1750, 2000 m). This low resolution, especially atthe OXY, could induce an error up to 25% of the vertical three layersof an OMZ. Note also that it has only been possible to consider theupper and lower boundaries, but not the lateral boundaries becauseof the insufficiently high horizontal resolution of the WOA2005data: therefore, in the present study, the three OMZ layers havethe same extent, horizontally. All OMZ dimensions and gradientswere performed systematically using the same Ferret calculationscript for: (i) horizontal extent, following the depths of minimumO2 concentration (the ‘‘Iso-minimum of O2” or ‘‘isominox”), be-cause, as we will be seen (cf. CORE thickness, Table 1), the lowestO2 concentrations can be observed at different depths. For theNMZ, the script calculates the NDEF maximum (‘‘isomaxndef”), byanalogy with the ‘‘isominox”; (ii) vertical thickness, by sequentialsingle integration over standard discrete sampling depths for eachlayer (OXY, CORE, LOG) and for the total OMZ layer (similar calcu-lations for NMZ); (iii) OXY and LOG O2 gradients by averaging fromthe OXY and LOG O2 gradient determined at each standard discretesampling depth by differences between each consecutive depth:i.e., (O2 z +dz � O2 z )/dz averaged over the whole thickness of theOXY and of the LOG.
In addition to the WOA2005 climatology, profiles and verticalsections from biogeochemical cruises have been used directly, withthe same or better accuracy (up to <1 lM for O2), to illustrate thecomparisons between: (i) different OMZs with representative sta-tions from the WOA2005 database (cf. Fig. 2): at 21�S, 71�W offChile; at 9�S, 85�W off Peru; at 12�N, 100�W in the ETNP; at15�N, 64�E in the AS; and at 15�N, 90�E in the BB; (ii) different cri-teria (CRIO, NDEF, NO�2 ; cf. Figs. 4 and 5) from process study data:S4BGC at 21�S, 71�W off Chile (Paulmier, 2005), and N7 at 15�N,64�E in the AS (US JGOFS); WOCE P21E at 17�S off Peru, andP19C at 90�W in the ETNP.
3. Results
The results presented concern the extents of the OMZs and theNMZs.
3.1. Extent of OMZs
The CRIO criterion including CORE (O2 <20 lM), OXY and LOG,applied to WOA2005 climatology, allows the identification(Fig. 1a), the evaluation of the vertical and horizontal structure(Fig. 2 and Table 1) and the seasonality (Fig. 3 and Table 2) of allthe OMZs. The following Sections 3.1.1–3.1.3 always refer to Table 1.
3.1.1. Identification of OMZsThis section always refers to Fig. 1a. The most intense OMZs in
the open ocean are identified by the suboxic conditions in their
CORE (O2 <20 lM: in red1). They are found mainly in the easternPacific (EP), and in the northern Indian (NI) semi-enclosed by thecontinents. In the EP, OMZs extend between 37�S and 52�N andfrom the coast out to 180�W (>10,000 km offshore); in the NI,OMZs extend from 23�N at the coast to 7�N (>1500 km south-wards) and including the area between 55�E and 100�E. In theAtlantic, LOZs have been detected in the North- and South-easternAtlantic Ocean (shades of yellow). These LOZs, with O2 P 20 lM(>40 lM in the North; >20 lM in the South, except in veryrestricted areas over the continental margin (O2 reaching17–18 lM), are much less intense than the OMZs in the Pacificand Indian Oceans, and are not considered in the present study.In the EP and NI, OMZs with distinct characteristics can be identi-fied: ENP in the North, and ESP in the South; AS in the West, and BBin the East. In the EP, ENP and ESP, OMZs are in contact horizon-tally, but neatly dissociated by three branches extending to theWest: ESP (0–37�S); ETNP (0–25�N); ESTNP (eastern subtropicalNorth Pacific; 25–52�N), the highest latitude for a permanentOMZ. There is no formation of OMZ at high latitude in the southernhemisphere, except in the ESP off Chile, but only up to 37�S. Verti-cally, these three branches can be clearly differentiated by their po-sition. A deepening of �150 m from the ESP (CORE centered at adepth of 365 m, with upper CORE isobaths contouring the OMZat 400 m depth) to the ETNP (with upper CORE isobaths at600 m), and of �430 m from the ETNP (530 m) to the ESTNP (withupper CORE isobaths at 1200 m). Note the dissymmetry betweenthe North and the South Pacific, due to a closed coastline to theWest-North for the ENP compared to an open coastline orientedSouth-East from the equator for the ESP. AS and BB are clearly dis-sociated horizontally by the southern end of India (and Sri Lanka),although with comparable isobaths around 200 m depth. Most ofthe OMZs are located in tropical latitudes (<25�); the ESP off Chileand the ESTNP OMZs being the only two located at higher latitudes.
Regionally, each OMZ presents some spatial variability not de-tailed here, as the two meridional AS components (Naqvi et al.,2006): intense in the East (<8 lM), associated with the Indian con-tinental margin; less intense in the central-western open ocean(>8 lM). In this study, the ESP OMZ is the only OMZ discussedmainly with respect to its three components (near the equator;off Peru; off Chile), and has been especially illustrated off Peruand Chile.
3.1.2. Vertical structure of the OMZsThe vertical OMZs structure is here described for each OMZ
layer. OMZs present differences in O2 concentration (for the CORE),thickness and depth range, and O2 gradient (for the OXY and theLOG).
The COREs of ESP near the equator and in the BB are the leastintense (O2 P 7 lM), with O2 values four times higher than in allother OMZ COREs. The difference in minimal O2 values in COREis especially marked between: the BB (10 lM) and the AS(2 lM); the ESP near the equator (7 lM) and off Peru (3 lM);and, in respect of the mean CORE O2 concentrations, between theESTNP (18 lM) and the ETNP (14 lM). In addition to the COREintensity, the ESP OMZ, off Chile and Peru, has a mean O2 contentfor OXY (89 and 81 lM, respectively) and for LOG (130 and113 lM, respectively) that is �20% higher than for the other OMZs.
The OMZs in the ETNP, the ESP off Peru and near the equator arethe thickest and at the greatest depth OMZs (>3000 m; Fig. 2a). TheOMZ off Chile is the thinnest (740 m) with the strongest OXY(2.1 lM/m). The CORE in AS OMZ is the thickest (>750 m). TheCOREs off Chile and Peru and in the BB are the shallowest (from160 m). The COREs in the ESP near the equator, the ETNP and the
Table 1Horizontal extent (Area), vertical characteristics (OXY; CORE; LOG) in terms of thickness and depth range, O2 concentration ([O2]) and O2 gradients for the main and most intense permanent OMZ regions in the open ocean, with maximalmixed and euphotic layers depth
OMZ regions Total OMZ Oxycline Core Lower O2 gradient (LOG) MixedLayerDepthe
m
Euphoticlayerf m
Area 106
km2 (%)aThickness m[Zmin; Zmax]b
Thicknessm (%)c
Mean [O2] lM(max [O2])d
O2 GradientlM/m (max)d
Thicknessm (%)c
[Cmin; Cmax]b
Mean [O2] lM(min [O2])d
Thicknessm (%)c
Mean [O2] lM(max [O2])d
O2 GradientlM/m (max)d
Global ocean 30.4 ± 3 3360 ± 800[10; 3370]
440 ± 170(13%)
65 ± 58 (202) �1.7 ± 0.6(�5.9)
340 ± 280(10%) [450–790]
15 ± 3 (2) 2580 ± 870(77%)
100 ± 43 (140) +0.04 ± 0.06(0.1)
– –
EasternPacific(EP)
EasternSouthPacific(ESP)
Chile: (18–37�S;70–82�W)
0.4 ± 0.1 740 ± 720[10; 750]
150 ± 50(20%)
89 ± 78 (238) �2.1 ± 0.8(�4.7)
160 ± 120(22%)[160; 320]
15 ± 2 (3) 430 ± 740(58%)
130 ± 38 (166) +0.03 ± 0.02(0.1)
44 60–120
Peru: (0–18�S;80–90�W)
0.6 ± 0.1 3740 ± 1020[10; 3750]
160 ± 40(4%)
81 ± 70 (214) �1.8 ± 0.6(�4.7)
340 ± 160 (9%)[170; 510]
13 ± 2 (3) 3240 ± 1010(87%)
113 ± 43 (150) +0.03 ± 0.02(0.1)
69 75–90
Equatorialcomponent:(0–18�S; 75–120�W)
4.7 ± 0.5 3360 ± 560[10; 3370]
270 ± 100(8%)
65 ± 56 (201) �1.7 ± 0.6(�3.5)
190 ± 170 (6%)[280; 470]
15 ± 2 (7) 2900 ± 520(86%)
105 ± 38 (143) +0.03 ± 0.02(0.1)
139 60–110
5.7 ± 0.6(19%)
3490 ± 660[10; 3500]
260 ± 100(7%)
66 ± 58 (238) �1.7 ± 0.6(�4.7)
190 ± 170 (5%)[270; 460]
15 ± 2 (3) 3040 ± 650(87%)
108 ± 39 (220) +0.03 ± 0.02(0.1)
148 60–120
EasternNorthPacific(ENP)
EasternTropicalNorth Pacific(ETNP):(0–25�N; 75–180�W)
12.4 ± 1(41%)
3560 ± 760[10; 3570]
310 ± 130(9%)
59 ± 55 (197) �1.8 ± 0.7(�5.9)
420 ± 290(12%)[320; 740]
14 ± 3 (2) 2830 ± 860(79%)
99 ± 43 (141) +0.04 ± 0.02(0.1)
103 30–90
Eastern Sub-Tropical NorthPacific(ESTNP):(25–52�N;75–180�W)
8.2 ± 1(27%)
2950 ± 760[20; 2970]
830 ± 160(28%)
76 ± 64 (240) �1.2 ± 0.3(�2.6)
230 ± 130 (8%)[850; 1080]
18 ± 1 (3) 1890 ± 810(64%)
100 ± 45 (141) +0.04 ± 0.02(0.1)
175 –
NorthIndian(NI)
Arabian Sea (AS):(7–23�N; 55–77�E)
2.5 ± 0.2(8%)
2980 ± 680[10; 2990]
230 ± 160(8%)
63 ± 58 (191) �1.6 ± 0.4(�3.3)
760 ± 340(26%)[240; 1000]
13 ± 4 (2) 1990 ± 770(67%)
93 ± 44 (127) +0.05 ± 0.03(0.1)
96 150–200
Bay of Bengal (BB):(8–20�N; 80–100�E)
1.6 ± 0.2(5%)
2400 ± 600[10; 2410]
170 ± 30(7%)
69 ± 62 (191) �1.9 ± 0.5(�3.3)
310 ± 160(13%) [180;490]
16 ± 2 (10) 1920 ± 670(80%)
85 ± 43 (126) +0.05 ± 0.02(0.1)
81 –
Values are calculated from annual and regional averages (WOA2005 database) using CRIO criterion for the definition of each layer. Note that for OXY and LOG Thickness, upper and lower limits correspond to [Zmin:Cmin] and[Cmax:Zmax], respectively.± Indicates: for Area columns, errorbar on the calculation mainly due to the horizontal resolution of the WOA2001 climatology; for other columns, classical standard deviation on the whole considered areas.
a % of each OMZ area on the total OMZ area.b Zmin and Cmin, and Zmax and Cmax are the upper and lower depth of the total OMZ and the CORE, respectively.c % of the OXY or CORE or LOG thickness on the total OMZ thickness.d Maximal concentration (for OXY at Zmin and LOG at Zmax) or absolute value of O2 gradient (for OXY and LOG O2 gradient), and minimal concentration for CORE.e Maximal depth from 0.03 kg m�3 density criterion (De Boyer Montégut et al., 2004).f Range of the maximal depth for the euphotic layer (from JGOFS 2003 database; for ESP off Chile, Ulloa, Pers. Com; for ESTNP and BB, no data available found).
118A
.Paulmier,D
.Ruiz-Pino
/Progressin
Oceanography
80(2009)
113–128
Oxygen (µM)
Dep
th (
m)
ef
BB
AS
ASBB
b
Zm
c
4469
Ze
d
608090
g
8196
h
175
(m)
50
100
150
200
250
350
300
50
100
150
200
250
350
300
0
500
1000
1500
2000
2500
3000
4000
3500
EA
ST P
AC
IFIC
NO
RT
H IN
DIA
N
a
0 40 80 120 160 200 240 0 40 80 120 160 200 240
ESPC
ESPPETNP
ETNP
ChilePeru
0
500
1000
1500
2000
2500
3000
4000
3500
103
Fig. 2. O2 profiles for 0–2700 m (a and e) and for 0–300 m (b and f), mean maximal mixed-layer (Zm: c, g) and euphotic layer (Ze: d, h) for the main OMZs in the Pacific (upperrow, a and b: ESP off Chile (21�S; 71�W) and off Peru (9�S; 85�W); ETNP (12�N; 100�W)) and the Indian (lower row, e and f: AS (15�N; 64�E); BB (15�N; 90�E)) Oceans fromWOA2005 data at representative locations for each OMZ. Horizontal striped segments indicate the lower OMZ limit (a and e). Horizontal lines represent the upper OMZ depth (band f). For acronyms, see in Fig. 1a.
A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128 119
ESTNP are the deepest (from 280 m down to 850 m). The meanCORE thickness of each OMZ is between 4 (AS) and 20 (ESP) timessmaller than the thickness of the total vertical OMZ structure. Thethickness of the CORE, but also of the OXY, relative to the total OMZthickness is quite comparable (�10%), except for the AS where theCORE thickness is three times larger than that of the OXY and forthe ESTNP where it is the contrary (1/3). The large thickness ofthe ESTNP OXY induces the less strong OXY (�1.2 lM/m). Gener-ally, LOGs in the EP OMZs are relatively thicker (>2800 m) and lessstrong with higher mean O2 concentrations (100–130 lM) than inthe NI (85–93 lM).
The euphotic layer in the ETNP is the shallowest (from30 ± 30 m deep) and in the AS (up to 200 ± 25 m), but with a meandepth for all the OMZs intercepting the OXY (Euphotic Layer col-umn; Ze in Fig. 2d and h). Note however that the information onthe euphotic layers is only indicative, on average, because of thehigh spatial and temporal variability of this parameter (up to a fac-tor of 2). The maximal mixed-layer depths off Chile and Peru, andin the BB and the AS are the shallowest (44–96 m); and for theESTNP, the ESP near the equator and the ETNP, the deepest (103–175 m; Zm in Fig. 2c and g). But, the maximal mixed-layer depthsfor all the OMZs intercept the OXY, hence allow the OMZ comepartially in contact with the ocean–atmosphere interface duringthe year. Because the relationship between factors derived fromclimatology ignores the probable temporal disconnect betweenstatistical tendencies, comparisons between Ze � Zm and OMZsshould be considered with much caution.
Despite differences, a common vertical structure can be seen forall the OMZs:
(i) OXY: strong (�1.7 lM/m; P1.2 lM/m), four times more oxy-genated (�65 lM) than CORE, shallow from a depth of 10–20 m,intercepted by euphotic zone and by the maximal annual mixed-layer depth; (ii) CORE: intense (1 6 O2 < 20 lM), highly O2-defi-cient (�15 lM, reaching minima <10 lM), extending over severalhundred meters (>300 m on average) between 160 and 1080 mdepth; (iii) LOG: one order of magnitude thicker (�2580 m), lessstrong (�0.04 lM/m), and 35% more oxygenated (�100 lM) thanin the OXY.
3.1.3. Horizontal extent of OMZsHorizontally, all OMZs extend (identified here by ‘‘isominox”
depth; Fig. 1a), over an area of 30.4 � 106 km2 (±10%), a significantsurface accounting for �8% of the present global ocean surface. TheETNP OMZ, covering 12.4 � 106 km2 (41% of the entire OMZs’ sur-face), is the largest (Table 1), followed by the ESTNP (27%) and theESP (19%) OMZs. The ENP OMZ (ETNP+ESTNP) covers 20.6 �106 km2, about 78% of the total Pacific OMZs. This difference in ex-tent between the ENP and the ESP OMZs has probably to be associ-ated with the so-called conveyor belt which is more impoverichedin O2 in the North than in the South Pacific. In the ESP OMZ, thecomponents near the equator covering a surface of 4.7 � 106 km2
and representing about 82% of the total ESP OMZ, appear moreimportant than the better known ESP off Peru and Chile. The small-est OMZs are those found in the Indian Ocean, in the AS and the BB
Fig. 3. O2 distribution (lM; at ±2 lM intervals) at depth where O2 concentration is minimal, according to the WOA2005 climatology and to the CRIO criterion (O2 < 20 lM inthe CORE) applied in spring (a), summer (b), fall (c) and winter (d). For OMZs acronyms, see in Fig. 1a.
120 A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128
(respectively 8% and 5% of the global OMZ surface). However, bothareas are only �30% lower than that of ESP OMZ.
Considering the EP and NI OMZs as permanent open-oceanOMZs (without taking into account the low seasonality: see herebelow), with a vertical extent of 3360 m (±800 m), OMZs representoverall a mean volume estimated at 102 ± 15 � 106 km3 (7 ± 1% ofthe ocean volume). The CORE (O2 < 20 lM) of all OMZs taken to-gether occupies a volume of 10.3 � 106 km3, about one tenth ofthat occupied by the all the OMZs as a whole, including OXY andLOG. In volume, the biggest OMZ COREs are in the ETNP and theAS, due to their large horizontal extent (representing almost halfthe total OMZ extents in the global ocean) and vertical extent(up to twice the mean thickness of the CORE), respectively.
3.1.4. Seasonality of OMZsThe climatological seasonal variability of the whole OMZ has
been analyzed for the total OMZ horizontal extent, their COREthickness and vertical depth range, and their O2 concentration inthe CORE. This variability is commented for the five OMZs alreadydescribed annually, and then for two new OMZs appearing season-ally. This whole section refers only to Fig. 3 and Table 2, unlessotherwise indicated, and to boreal seasons.
Fig. 3 shows at the global scale that the five main OMZs, alreadydescribed from Fig. 1a (ESTNP, ETNP, ESP, AS, BB), are always pres-ent and with comparable horizontal extents (32.2 < 34.6 �106 km2) and features for each of the four seasons. Therefore, sea-sonality would hardly affect the OMZs horizontal extent (�10% be-tween 0.1 and 3.0 � 106 km2), the CORE thickness and verticaldepth range (330–340 m with Cmin� 440–470 m; cf. note b, Table 2),
and the O2 concentration (Mean [O2] � 15 ± 1 lM; Min[-O2] � 0 lM). Among the seasonally permanent OMZs, the ETNPand ESP OMZs, as at the global scale, do not show significant sea-sonal changes, although the extreme western end could detachfrom the rest of the OMZ in: summer for the ETNP (at 185�W;Fig. 3b); fall for the ESP (at 130�W; Fig. 3c).
However, for the other permanent OMZs, a seasonal variabilityhas been detected, at least for one of the structural components,horizontally or vertically or in intensity, and here illustrated themost completely by all the structural components of the AS OMZ.During the spring–summer transition, the AS OMZ CORE presentsa thickening of 20% (from 640 m to 790 m), associated with ashoaling from 280 to 220 m of the upper CORE limit. This thicken-ing is associated with a CORE intensification (>30%, from 16 lM to12 lM for the mean O2 concentrations), largely confirmed by theminimal O2 concentrations decreasing from 1 lM to 0.1 lM. Hori-zontally, on the contrary, the AS OMZ presents a contraction of�10% (from 3 to 2.7 � 106 km2). During the summer–fall–winter–spring transition, the variability is opposite. The AS OMZ CORE con-tracts vertically by 20% (from 790 to 720 m, then 710 m, then640 m, for the four mentioned seasons, respectively), with a deep-ening of the OMZ CORE upper limit by 60 m (from 220 m to 280 mdepth). The CORE becomes less intense by �30%, with O2 concen-trations increasing from 12 lM to 13 lM, then to 16 lM. Horizon-tally, the OMZ extends by 10%, from 2.7 to 3 � 106 km2.
This seasonal tendency, observed for the AS and especially forthe marked spring–summer transition, can also be observed forthe ESTNP, the ESP and the BB. But the seasonal changes are ob-served only in some of the structural components, and only in
Tabl
e2
Seas
onal
OM
Zch
ange
sin
hori
zont
alex
tent
(Are
a),i
nCO
REth
ickn
ess
and
mea
nO
2co
ncen
trat
ion
([O
2])
for
the
mai
nO
MZ
regi
onin
the
open
ocea
n
OM
Zre
gion
sTo
tal
OM
Zar
ea10
6km
2C
ore
thic
knes
sm
(Cm
in)b
Cor
em
ean
[O2]l
M(m
in[O
2])
c
Win
ter
Spri
ng
Sum
mer
Fall
Win
ter
Spri
ng
Sum
mer
Fall
Win
ter
Spri
ng
Sum
mer
Fall
Glo
bal
ocea
n34
.3±
334
.6±
332
.2±
332
.8±
333
0±
280
(440
)34
0±
280
(470
)34
0±
300
(450
)34
0±
280
(440
)15
±1
(0)
15±
1(0
)15
±1
(0)
15±
1(0
)Pe
rman
ent
OM
Zfo
ral
lse
ason
sES
PC0.
3±
0.1
0.2
±0.
10.
2±
0.1
0.2
±0.
114
0±
110
(180
)12
0±
110
(160
)20
0±
100
(150
)17
0±
120
(150
)15
±1
(5)
15±
1(3
)13
±1
(1)
15±
1(0
.9)
ESPP
0.6
±0.
10.
6±
0.1
0.6
±0.
10.
6±
0.1
300
±19
0(1
80)
350
±15
0(1
50)
340
±16
0(1
80)
360
±17
0(1
60)
13±
1(0
.8)
13±
1(2
)12
±1
(0.5
)13
±1
(1)
ESPE
q4.
9±
0.5
4.7
±0.
55.
0±
0.5
4.4
±0.
519
0±
170
(270
)18
0±
170
(290
)17
0±
160
(280
)19
0±
180
(270
)14
±1
(5)
16±
1(8
)15
±1
(5)
15±
1(5
)ES
P6.
0±
0.6
6.0
±0.
66.
1±
0.6
5.6
±0.
619
0±
170
(260
)18
0±
170
(280
)17
0±
170
(270
)19
0±
180
(250
)14
±1
(0.8
)15
±1
(2)
15±
1(0
.5)
15±
1(0
.9)
ETN
P12
.6±
113
.6±
112
.7±
113
.5±
141
0±
300
(320
)44
0±
300
(330
)43
0±
310
(320
)40
0±
280
(320
)14
±1
(0.2
)13
±1
(0)
14±
1(0
)14
±1
(1)
ESTN
P8.
3±
19.
2±
18.
6±
18.
0±
120
0±
130
(870
)24
0±
130
(890
)22
0±
130
(850
)25
0±
140
(840
)17
±1
(0.4
)17
±1
(0.7
)17
±1
(4)
17±
1(2
)A
S2.
7±
0.2
3.0
±0.
22.
7±
0.2
2.7
±0.
271
0±
350
(230
)64
0±
340
(280
)79
0±
350
(220
)72
0±
400
(240
)13
±1
(0)
16±
1(1
)12
±1
(0.1
)13
±1
(0.3
)B
B1.
6±
0.2
1.7
±0.
21.
55±
0.2
1.7
±0.
237
0±
170
(170
)27
0±
180
(200
)20
0±
160
(200
)38
0±
190
(160
)15
±1
(2)
16±
1(3
)17
±1
(3)
15±
1(1
)O
MZ
wit
hse
ason
aldi
sapa
riti
onW
BS
2.2
±0.
20.
2±
0.2
0.3
±0.
20.
2±
0.2
170
±16
0(6
90)
––
–18
±1
(15)
––
–G
A0.
4±
0.1
0.7
±0.
10.
1±
0.1a
1.1
±0.
116
0±
150
(670
)40
±10
0(7
70)
210
±16
0(8
50)
180
±23
0(8
40)
19±
1(1
3)18
±1
(10)
18±
1(1
4)18
±1
(8)
Val
ues
are
calc
ula
ted
from
seas
onal
and
regi
onal
aver
ages
(WO
A20
05da
taba
se)
usi
ng
the
CR
IOcr
iter
ion
for
the
CO
RE
defi
nit
ion
.For
OM
Zsac
ron
yms,
cf.t
he
end
ofth
ete
xt.F
orer
rorb
ars
(±),
cf.n
ote
ofTa
ble
1.a
GA
OM
Zco
nsi
dere
das
disa
ppea
red
due
toth
eu
nce
rtai
nty
.b
C min
=C
OR
Eu
pper
lim
itde
pth
(Cf.
Tabl
e1)
.c
min
[O2]
=m
inim
alO
2co
nce
ntr
atio
n;
ofte
nbe
low
the
sign
ifica
tivi
ty±2
lM
.
A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128 121
some seasonal transitions. Indeed, between spring and summer,the ESTNP OMZ contracts horizontally by �7% (from 9.2 to8.6 � 106 km2). The ESP OMZ off Chile thickens by 67% (from120 m to 200 m) with an intensification of its CORE by >15% (from15 lM to 13 lM). Between fall and winter, the OMZ CORE in theESP off Peru contracts vertically by nearly 20% (from 360 m to300 m), with a deepening of the CORE upper limit of 20 m (from160 m to 180 m). Between spring and summer, the OMZ CORE inthe ESP at the equator intensifies by �7% from 16 lM to 15 lMfor the mean O2 concentrations, and from 8 lM to 5 lM for theminimal O2 concentrations. Finally, always between spring andsummer, the BB OMZ contracts horizontally by �10% (from 1.7 to1.55 � 106 km2).
In addition to the permanent OMZs, an OMZs map for each sea-son allows the detection of two new OMZs that disappear season-ally, and which therefore cannot be observed on an annual map(Fig. 1a):
(i) in the West Bering Sea (WBS: 45–65�N; 175–210�W)appearing mainly in winter (Fig. 3d; 2.2 � 106 km2), andmore or less disappearing in the other seasons (Fig. 3a–c;<0.3 � 106 km2). This WBS OMZ reaches 7% of the totalOMZs’ surface (2.2 � 106 km2), which is comparable to theAS OMZ surface (2.5 � 106 km2: Total OMZ Area in Table1), and with a deep (between 690 and 1100 m) and lessintense (mean O2 of 17–18 lM) CORE;
(ii) in the Gulf of Alaska (GA: 52–65�N; 120–175�W) appearingin fall–winter–spring (Fig. 3c, d, a; >0.4 � 106 km2), with amarked presence in fall and spring (1.1 and 0.7 � 106 km2,respectively) and an attenuated presence in winter(0.4 � 106 km2). GA more or less disappears in summer(Fig. 3b; 60.1 � 106 km2). Therefore, the GA OMZ shouldpresent, as the other permanent OMZs generally do, a hori-zontal contraction between spring and summer by a factorof 7 (from 0.7 to 0.1 � 106 km2), whereas its CORE thickens,up to a factor of >5 (from 40 to 210 m). Note that the GAOMZ is in contact with the ESTNP mainly in the fall, as wellas in winter and spring (Fig. 3a, c, d), probably correspondingto a northern prolongation of the ESTNP associated with aconnection and an O2 deficit transfer between both OMZs.In fact, according to the CORE vertical depth range between670 and 1060 m depth, with a CORE upper limit (e.g., Cmin
= �840 m in spring), GA and ESTNP are at comparabledepths, and present less intense COREs (Core Mean [O2] of18–19 lM). Taking into account the WBS (in winter) andthe GA (in fall and spring), the total OMZs surface increasesup to �10% rising to 33.5 � 106 km2.
Thus, in the OMZs in which a significant seasonality could beobserved, there is a marked spring–summer transition associatedwith, on average: (i) CORE thickening of �4.4%, generally associ-ated with a CORE upper limit shoaling (between 10 and 30 mdepth); (ii) a horizontal OMZ contraction by �1.3%; (iii) COREintensification associated with a diminution in the mean O2 con-centration up to 4 lM, as in the AS; (iv) OXY and LOG with higherO2 concentration less intense, associated with an oxygenation in-crease up to 9 lM and 6 lM, respectively, as in the BB OMZ (notshown in Table 2). Especially during the fall–winter transition,the OMZs generally present a more gradual seasonality and oppo-site to the spring–summer transition.
These observations of vertical thickening and CORE intensifica-tion, observed in spring–summer, are in agreement with an in-crease of hypoxia (less oxygenation) reported during the sameperiod by Kamykowski and Zentara (1990). This seasonality alsomatches the local observations of OMZ formation over the shelfand/or shoaling in spring–summer, associated with a stronger
Tabl
e3
Com
pari
son
betw
een
NM
Zan
dO
MZ
from
the
CRIO
crit
erio
nof
this
stud
y,fo
rth
eho
rizo
ntal
exte
nt(A
rea)
and
vert
ical
(Thi
ckne
ss)
char
acte
rist
ics
ofth
em
ain
perm
anen
tO
MZ
regi
ons
inth
eop
enoc
ean
Reg
ion
sA
rea
106
km2
Thic
knes
sm
Mea
n[N
DEF
]in
NM
Zl
M(m
ax[N
DEF
])d
NM
Z(%
)aO
MZ
(th
isst
udy
)N
MZ
T(%
)b
[Zn m
in;
Znm
ax]c
OM
ZC
ore
(Fro
mTa
ble
1)To
tal
OM
Z(F
rom
Tabl
e1)
Glo
bal
ocea
n15
.0±
1(4
9%)
30.4
±3
230
±32
0(6
8%an
d7%
)[2
30;
460]
340
3360
12±
1(2
9)Ea
ster
nPa
cifi
c(E
P)Ea
ster
nSo
uth
Paci
fic
(ESP
)C
hil
e:0.
4±
0.1
(100
%)
0.4
±0.
116
0±
80(1
00%
and
22%
)[8
0;24
0]16
074
015
±2
(27)
Peru
:0.
6±
0.1
(100
%)
0.6
±0.
122
0±
70(6
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thIn
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mn
OM
Z.
122 A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128
upwelling (e.g., off Chile; Graco, 2002). But here, the OMZs season-ality appears more complex. In fact, vertical thickening is associ-ated with horizontal contraction during spring–summer, andCORE intensification with more oxygenated OXY and LOG; and in-versely in fall–winter. The anti-correlated seasonal variability inthe intensity of the CORE and the OXY–LOG oxygenation suggestprobable spread of the O2 deficit between the CORE and its bound-ary layers. This proposed seasonality cannot be detailed furtherhere, mainly because of a lack of data to identify significant ten-dencies for each season.
3.2. Extent of the denitrification (NMZs) zone
This whole section refers always to Table 3, unless otherwiseindicated.
3.2.1. IdentificationDenitrification regions (NMZs) in the open ocean have been
identified on a global scale using the ‘NDEF > 10 lM’ criterion(Fig. 1b). As for OMZs, NMZs are found in the EP, between 37�Sand 25�N and from the coast out to 160�W (>8000 km offshore),and more confined in the NI, from 23�N at the coast to 8�N(>1400 km southwards) and including the area between 55� and90�E only. But a NMZ is also found in the Arctic Ocean, mainly asso-ciated with the large western continental shelves, as in the Chukchiand Beaufort seas, in agreement with the N* analysis by Gruber andSarmiento (1997). Except the Arctic region (high latitude: >60�N),where there is no water-column OMZ (Fig. 1a), four main NMZscan be distinguished in the ETNP, ESP, AS and BB OMZs, but notin the ESTNP.
Regionally, the ETNP NMZ is much more confined to thecoast (out to 140�W) than the OMZ, and presents a dissociated lo-cal NMZ far offshore near the equator and 140�W. The highestNDEFs (up to 22 lM) are confined close to the coast, whereas therest of the ETNP presents NDEFs mainly between 11 and 18 lM.The ESP NMZ is also more restricted to the south (between 10�Sand 37�S). The NMZ off Peru is the most intense (with higher NDEFup to 24 lM) close to the coast, where the rest of the ESP presentsNDEFs mainly between 11 and 18 lM. The AS NMZ covers quitewell the OMZ extent with a weak extension restricted to the northof 10�N and with homogenous NDEFs of �12 lM (highest values>19 lM in the northeastern part close to the coast). Contrary tothe AS, the BB NMZ extent is very restricted close to the eastcoast of India between 80�E and 90�E, with a low mean NDEF of�11 lM.
3.2.2. Vertical extent of the denitrification (NMZs) zonesVertically, the AS and ETNP NMZs are characterized as the deep-
est (lower limit between 480 and 590 m depth) and thickest (be-tween 260 and 400 m depth). The ESP NMZ is the shallowest(upper limit from 50 m; lower limit from 220 m) and one of thethinnest (�230 m), with the highest NDEF (up to 27 lM off Chileand 24 lM off Peru). The BB NMZ is also one of the shallowest(upper limit at 130 m) and the thinnest (90 m), with the lowestNDEF for an NMZ (11 lM). There is no NMZ in the ESTNP(NDEF < 10 ± 2.5 lM). The Arctic NMZ without a correspondingOMZ, is the shallowest (from 70 m depth), the thinnest (90 m, asfor the BB) and one of the most intense (13 nM up to 39 lM) NMZs.
The vertical mean NMZ structure (Table 3) is confirmed by theillustrating profiles (off Chile and in the AS; Fig. 4) and sections (offPeru and in the ETNP; Fig. 5) of NDEF and NO�2 . Regarding the typ-ical profile off Chile, the NMZ (Fig. 4b) has a thickness of 145 m be-tween 150 and 295 m depth, in agreement with the NO�2 maximum(Fig. 4c). For the AS, the NMZ (Fig. 4e) has a thickness of 370 m be-tween 230 and 600 m depth, that appears largely thicker than sug-gested by the NO�2 maximum (Fig. 4f). The thickness of the NMZ off
Fig. 4. Profiles of O2 (a and d), NDEF (b and e: NDEF>10 lM shaded) and NO�2 (c and f: NO�2 > NO�2max=2 lM shaded) at representative locations (21�S; 71�W) off Chile (top row)and (15�N; 64�E) in the AS (bottom row). In a and d, backgrounds correspond to vertical extent of the OMZ (dashed area) and of the CORE (grey area). A typical mean vertical O2
profile from WOA data ‘outside OMZs’ (classical O2 minimum) is shown in pointed line.
Fig. 5. Vertical sections of O2, NDEF and NO�2 (a–c: Peru at 17�S; d–f: ETNP at 90�W). Contours (thick black lines) correspond to: O2 = 20 ± 2 lM (a,d); NDEF = 10 ± 2.5 lM(b,e); NO�2 ¼ NO�2max/2 lM (c and f).
A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128 123
124 A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128
Peru (Fig. 5b) and in the ETNP (Fig. 5e) are slightly larger than sug-gested by the NO�2 maximum (Fig. 5c and f). Consequently, for allthe NMZs, the vertical thickness appears generally higher than sug-gested by the NO�2 maximum.
3.2.3. Horizontal extent of the denitrification (NMZs) zonesHorizontally (Fig. 1b; Table 3), all NMZs, without taking into ac-
count the Arctic NMZ, extend over an area of 15.0 � 106 km2 (±7%),i.e., �4% of the ocean surface. The ETNP NMZ, covering 7.8 �106 km2 (52% of the entire NMZs’ surface), is the largest, followedby the ESP NMZ (28%). The NMZ in the northern hemisphere coversabout 65% of the total Pacific NMZs. The smallest NMZs are thosefound in the Indian Ocean: the AS (15%), and especially the BB(5% of the global NMZs’ surface). The Arctic NMZ is not taken intoaccount here, because it does not have a corresponding water-col-umn OMZ, although it covers a significant area of 5.4 � 106 km2
(one-third of all the other NMZs).NMZ extent can be compared qualitatively to the NO�2 maxi-
mum extent (Figs. 4 and 5). Off Peru, the NMZ extends westwards6�1600 km from the coast, i.e., much farther than the NO�2 maxi-mum (Fig. 5b and c). Likewise, for the ETNP, the NMZ extendssouthwards 6�1000 km from the coast, i.e., almost as far as forthe NO�2 maximum (Fig. 5e–f). The NO�2 maximum, although witha smaller extent, confirms the NMZ extent and the presence ofdenitrification.
Total NMZs’ volume, considering a vertical extent of �230 m,represents a mean volume of �3.45 ± 0.05 � 106 km3 (�0.03 ±0.001% of the ocean volume). In volume, the biggest NMZs are inthe ETNP (58% of the total NMZ volume) and the AS (27%), as forthe OMZs. The smallest NMZ volume is in the BB, 2% of the totalNMZ. The NMZ seasonality could not be studied at all, because ofinsufficient availability of data for each season.
4. Discussion
OMZs and NMZs characterized in this study were compared be-tween themselves, and with the classical O2 minimum and previ-ous evaluations. Then, the choice of a criterion to take intoaccount the entire OMZ volume associated with OMZs is discussed.
4.1. Comparison between OMZs and NMZs extents
To characterize the differences between the volume of OMZsand denitrification zones, the extents of the OMZs and NMZs werecompared. These comparisons are first illustrated with profiles offChile and in the AS (Fig. 4) and with vertical sections off Peru and inthe ETNP (at 17�S and 90�W; Fig. 5), then confirmed on a globalscale.
Locally, and vertically, on a typical OMZ profile off Chile, theCORE and NMZ are located between 160 and 320 m depth, and be-tween 150 and 295 m depth, respectively (Fig. 4a and b). The NMZwould thus underestimate the OMZ CORE thickness (160 m) byabout 9 ± 3%. For the AS, the CORE and NMZ are located between240 and 1000 m depth, and between 230 and 600 m depth, respec-tively (Fig. 4d–e). The vertical NMZ extent (�370 m) is more thantwo times smaller than the CORE extent. Off Peru, the CORE andNMZ are located on average between 170 and 510 m depth, andbetween 120 and 350 m depth, respectively (Fig. 5a–b). The NDEFdenitrification criterion therefore underestimates the OMZ COREthickness (340 m) by 30% (110 m). For the ETNP, the CORE thick-ness is 420 m, between 320 and 740 m depth, but the NMZ is15 ± 4% thinner and 1.3 times shallower (less than 250 m depth;Fig. 5d–e). Horizontally, the area of the OMZ CORE off Peru areaextends westwards out to �1800 km from the coast, which is 10%farther than for the NMZ (Fig. 5a–b). Likewise, for the ETNP, the
OMZ CORE extends southwards out to �3000 km from the coast:i.e., almost three times farther than for the NMZ (Fig. 5d and e).
On a global scale, the NMZ evaluation presents the same ten-dency to underestimate the OMZ CORE extent than was previouslynoted for each OMZ. Horizontally, OMZs (Fig. 1a) correspond toNMZs (Fig. 1b) in the ETNP, ESP, AS and BB, but the extent of theNMZs is more restricted than that of the OMZs out only to2000 km offshore in the EP, and only 1000 km southwards fromthe coast in the NI. The ETNP NMZ is about 2500 km closer to thecoast than the OMZ, and the ESP NMZ is limited to the southernpart, between 10� and 40�S, about 1000 km less extended towardsthe equator than the OMZ. The global NMZs area extent is15 � 106 km2, two times less (49%) than that of the overall OMZs(see note a, Table 3). For each OMZ, the same tendency to the under-estimation of the OMZ by the NMZ was observed between 37% inthe BB and 100% in the ESP off Chile and Peru. Vertically, all theOMZ COREs are associated with denitrification detected by thepresence of an NMZ (NDEF P 11 lM), but underestimated byNMZ by a factor of �1.5, between 0% in the ESP off Chile (100% ofthe CORE) and 68% in the ESP near the equator (32% of the CORE).
In synthesis, for all OMZs (Tables 1 and 3), the NMZ underesti-mates the OMZ extent by the following factors: (i) horizontally, be-tween 1 and 3 (weighted average: �2); (ii) vertically, between 1and 7 (weighted average: �1.5) for the CORE and �15 for the totalOMZ including OXY and LOG. In volume, OMZs (7% of the oceanicvolume) should be underestimated, by the denitrification criteria,by a factor of �3 for the CORE and of �30 for the total thickness.
4.2. Comparisons between OMZs–NMZs and previous evaluations
The OMZs’ structure is relatively different from those of the‘‘classical O2 minima”, found in all the oceans and between500 m and 2500 m depth (mean average depth about 1500 m;Wyrtki, 1962). All OMZs attaining the lowest CORE O2 concentra-tion of 2 lM are >50 times more intense than classical O2 minima,which are characterized by O2 concentrations of �50 and �200 lMfor the Pacific and Atlantic Oceans, respectively (WOA2005 data-base). OMZs, which may be located from 10 m depth, are 50 timesshallower and with a vertical extent over hundreds of meters,whereas even if the classical O2 minima are present in all oceans,the most intense OMZs are restricted to the EP and NI Oceans.
These differences between OMZs and classical O2 minima areshown for the ESP off Chile and for the AS (Fig. 4a and d). TheESP OMZ (Fig. 4a) CORE off Chile is between 160 and 320 m depth,with O2 reaching <1 lM, whereas the classical O2 minimum is be-tween 1200 and 1600 m depth and with a minimum O2 concentra-tion of about 40 lM. The situation off Chile is unique, presentingtwo differentiated O2 minima, one corresponding to the OMZ andthe other to the classical O2 minima. The classical O2 minimumoff Chile, although five times less intense (�100 lM), may corre-spond, by hemispheric symmetry in the EP, to the deep ESTNPOMZ (CORE up to 1080 m). On the AS OMZ (Fig. 4d), CORE is lo-cated between 240 and 1100 m depth, with O2 also reaching thedetection limit (<1 lM), whereas the classical O2 minimum is at2000 m depth, with a O2 minimum of �50 lM.
For OMZs (Fig. 1a, Table 1), the main documented extent, basedon O2 data all focused in the last decades, was estimated by differ-ent criteria for the O2 concentration: at the global scale for thetropical Pacific (ESP, ETNP), by Karstensen et al. (2008); from localstudies on the vertical extent by Anderson et al. (1982) for theETNP, ESP off Peru, and for the AS, by Morrison et al. (1999).
Horizontally, OMZ CRIO evaluation, based on the suboxic condi-tion O2 < 20 lM, corresponds qualitatively to the same regions iden-tified by the hypoxia (O2 < 8 lM) map (Kamykowski and Zentara,1990), except for the offshore ESP near the equator and ESTNP com-ponents. This relatively global agreement suggests that the CORE of
A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128 125
all the OMZs approaches hypoxia or at least O2 6 10 lM (Table 1).Moreover, with WOA2005 climatology and CRIO, the ESTNP andETNP OMZs are clearly dissociated, because OMZ extents have beenderived from the ‘‘isominox” calculation following the O2 minimumin the OMZ CORE. This dissociation between ESTNP and ETNP is inagreement with the frequency diagram of the number of hypoxiaobservations (Kamykowski and Zentara, 1990), showing dissocia-tion between the tropical (between 0� and 30�N) and subtropical(between 30� and 52�N) north latitudes. The OMZ CRIO evaluationis also in agreement with the description of Karstensen et al.(2008), especially in the eastern tropical Pacific. Note that OMZs ex-tend far into the open ocean (>8000 km for ESTNP and, closer to theequator, >10,000 km for ETNP); that is �30 times farther offshorethan the extent of the OMZs in contact with the seafloor(1148 � 106 km2; Helly and Levin, 2004). Although their extentwould always cover the coastal seafloor, the OMZ extent in the openocean is not correlated with the sedimentary extent of each OMZ.
Vertically, in all previous work on the O2 deficit, only OMZ COREhas been considered, but OXY and LOG have not been taken intoaccount. OMZ CORE thickness is globally in agreement with theestimates (O2 < 4.5 lM) of Karstensen et al. (2008) for the easterntropical Pacific (ESP, ETNP). Locally, the OMZ CORE thicknesses arein agreement within ±7% for the ESP off Peru (340 ± 160 m), butonly within 30 ± 7% for the ETNP (420 m), which is higher thanthe previous estimates (Anderson et al., 1982) evaluated from atwice as constraining O2 criterion (<10 lM) than CRIO. For theAS, the thickness (760 ± 340 m) is in agreement with that of a pre-vious study on the whole basin (O2 < 4.5 lM; Morrison et al.,1999), although using an O2 criterion even more constraining, bya factor of 4, than CRIO. The highest difference in thickness is thenmainly attributable to the studies based on local cruises, hence notrepresentative of the whole OMZ basins as defined herein.
In volume, the global OMZs CORE is about seven times largerthan the usually considered suboxia volume (0.1% of the oceanicvolume) proposed in Codispoti et al. (2001). For each oceanic basin,the OMZs CORE appears �16, �1000 and �120 times larger thanthat of the OMZs in the North (0.44 � 106 km3) and South(0.001 � 106 km3) Pacific, and Indian Ocean (0.002 � 106 km3), esti-mated by Karstensen et al. (2008) with the more constraining O2
< 4.5 lmol/kg condition, respectively.For NMZs (Fig. 1b; Table 3), volume comparison with the results
of previous denitrification extent studies reported in the literatureis not possible, because of the lack of information in the verticaldimension for a whole OMZ basin. At the global scale, our NMZssurface is about two times larger than the evaluation from Hattori(1983), mainly because the BB and the ESP near the equator and offChile were not considered. Locally, denitrification comparisonswere made only for the ETNP, the ESP off Peru, and the AS(Fig. 1a; Table 3). The ETNP NMZ (7.8 � 106 km2: Table 3) is about14% more extensive, and by factors 2.5 and 7, compared with thedenitrification surface evaluated by Goering et al. (1973), Clineand Richards (1972) and Codispoti and Richards (1976), respec-tively. The NMZ off Peru (0.6 106 km2) is about 1.8 times lessextensive than the denitrification surface evaluated by Codispotiand Packard (1980). The AS NMZ (2.3 � 106 km2) is �46 timesmore extensive than the denitrification surface evaluated by Deus-er et al. (1978). These comparisons do not only document the wayin which the presence of denitrification is determined, but also thespatial documentation and sampling strategy; previous studiesbased on cruises were generally more localized than the horizontalestimate made here for the whole OMZ basin.
4.3. Why denitrification criteria could not delimitate the entire OMZ?
The principal studies and evaluations in OMZs are focused onthe limited volume in which denitrification occurs, mainly in the
CORE. But the presence of denitrification did not allow the delim-itation of the entire volume associated with the OMZ perturbation.Two main reasons may be given: (i) denitrification does not exactlycorrespond to the CORE volume, which is intrinsically related tothe denitrification process; (ii) denitrification is probably not theonly important biogeochemical process associated with the OMZs.
The first difficulty is due to the determination of different vol-umes for the canonical (i.e. classically anaerobic) denitrification.The O2 threshold value, beneath which denitrification occurs, isvariable, from <0.8 lM in the eastern tropical Pacific (Goering,1968) to <20 lM in an ENP fjord (Smethie, 1987), and seems to de-pend on the region and on each local denitrifying bacteria commu-nity. Thus, the same criterion cannot be applied to determine thedenitrification volume for all the OMZs. In addition, the determina-tion of denitrification is often performed using different criteriaand at least three parameters (NDEF, NO�2 peak, O2 conditions),which do not describe the same volume (see Figs. 4 and 5).
The second difficulty is due to OMZ CORE underestimation bycanonical denitrification criteria (cf. Section 4.1). Denitrificationoccurs at O2 concentrations that are always less than 20 lM(Smethie, 1987). Thus, the canonical denitrification criteria couldunderestimate the OMZ CORE volume (O2 < 20 lM) only, and, afortiori, the total OMZ volume including OXY and LOG. In addition,the basic explanation of the OMZ CORE underestimation by theNMZs extent is that denitrification and hence NMZ detection ismainly controlled by the low level of O2 in the OMZ CORE, to whichdenitrifying bacteria would be very sensitive (Codispoti et al.,2001). Indeed, the ESP (especially off Chile and Peru) and the ETNP,which form intense NMZs (22 6 NDEFmax 6 27 lM), correspond tothe most intense OMZ CORE (2 6 O2 min 6 3 lM). The BB NMZ, themost restricted compared to the other OMZs and the least intenseNMZ (mean NDEF � 11 lM), is associated with the least intenseOMZ CORE (O2 always >10 lM). In the same way, the ESTNPOMZ, which does not have an NMZ (NDEF always <10 lM), corre-sponds to the less intense (Mean [O2] = 18 lM) and deeper (below850 m) OMZ CORE and the thickest OXY. Therefore, the absence ofan NMZ (ESTNP) or a low NDEF (BB) could be mainly due to aslightly more oxygenated OMZ (>2 lM of O2 compared with theother OMZs), but also to a lower level of bacterial activity becauseof a lesser supply of organic matter, as well as because of the coldand different environmental conditions. The ESTNP is the deepest(sinking organic matter is largely already degraded) and the cold-est OMZ (3 < 5 �C instead of >15 �C for the other OMZs). The BB ishighly subject to the continental influence of two of the world’sbiggest rivers (Brahmaputra, Ganges), which impose hydrologicaland biogeochemical conditions (e.g. temperature, salinity, organicmatter quality, bacteria composition) that are very different fromthe marine ones.
On the other hand, an ‘‘OMZ border-specific denitrification”can appear at the OXY of all OMZs with O2 > 20 lM, and could ex-plain why the NMZ would be slightly shallower than the OMZCORE (cf. Figs. 4 and 5). This specific denitrification, off Peru,was suggested by Codispoti and Christensen (1985), supportedby dN15 analysis in the AS (Naqvi et al., 1998), and recentlynamed OLAND (oxygen-limited autotrophic nitrification–denitrifi-cation: non-canonical denitrification from NO�2 produced by cou-pled nitrification; Brandes et al., 2007). Moreover, it is known thatdenitrification can proceed in the presence of O2 (Zehr and Ward,2002), outside the CORE boundaries, at a thin OXY but also at athick LOG (Li et al., 2006). This hypothesis could be confirmedby the potential existence of an oxygenated denitrification nearO2 saturation (>200 lM; Patureau et al., 1994). In this case, deni-trification criteria could overestimate OMZ CORE volume, orneglect to take into account the volume in which non-canonicaldenitrification (as OXY and LOG) or other biogeochemicalprocesses could occur.
126 A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128
The second reason why denitrification could not delimitate theentire OMZ is probably due to the existence of other biogeochem-ical processes related to the N cycle, which could locally affectNDEF and NO�2 in the O2 minimum. Consequently, from indirectindices as NDEF, it is difficult to capture, just the denitrificationprocess. In OXY and/or LOG, nitrification, remineralization, OLAND(cf. above), anammox could appear (e.g., Smethie, 1987; Wardet al., 1989; Paulmier et al., 2006; Thamdrup et al., 2006; Brandeset al., 2007). Photosynthesis could also occur near the OXY, becauseof the availability of light, as suggested by the secondary fluores-cence peak associated with Prochlorococcus and Synechococcuscommunities (e.g., Liu et al., 1998). Among the biogeochemicalprocesses, nitrification can be extremely active above (OXY) andbelow (LOG) the OMZ CORE (Anderson et al., 1982), and coexis-tence between denitrification and an aerobic process is possible(e.g., nitrification; Farias et al., 2007). More complex mechanismscould also affect the nitrogen cycle, such as the recently discoveredanammox reaction (NHþ4 þNO�2 ! N2 under anaerobic conditions;Kuypers et al., 2003). Consequently, a denitrification criterion doesnot allow the determination of the volume associated with all thebiogeochemical processes occurring in the entire three OMZ layers.NDEF may also be intensified by benthic denitrification, whichcould be more intense than in the water column, as observed inthe eastern AS OMZ on the continental margin (Naqvi et al.,2000). The NMZ detected in the Arctic Ocean was found mainlyon the large western continental margins, whereas no ArcticOMZ has been detected in the water column. This would be asso-ciated with a high level of denitrification in the suboxic–anoxicsediments (e.g., in the Bering, Chukchi and Beaufort Seas; Devolet al., 1997), which transmits a high NDEF signal detected here inthe water column (as for NO�2 ; Kamykowski and Zentara, 1991).The Arctic NMZ would also be associated with a horizontal advec-tion from the North Pacific (Yamamoto-Kawai et al., 2006). Thisimplies both that: (i) a less intense OMZ with O2 > 20 lM, as theLOZs in the eastern Atlantic, could be formed without water-column canonical denitrification; (ii) an NMZ could be formedwithout intense (O2 < 20 lM) water-column OMZ, as in the Arctic.
Due to the potential co-existence of different OMZ-specific pro-cesses, the use of the same criterion, directly based on O2 distribu-tion, as CRIO, could be better adapted to consider the influence ofthe whole OMZ and its specific biogeochemical processes. In par-ticular, CRIO avoids the underestimation of the biogeochemicalactivities linked to nitrogen cycle but also to carbon remineraliza-tion and to O2 consumption, at the OXY and LOG. Based on a sub-oxic criterion for the CORE, CRIO generally corresponds to thevarious definitions of the OMZ: oxygen-minimum layer (OML;Goering, 1968), oxygen-deficient zone or layer (ODZ or ODL; Naqviet al., 2006). In addition, the common characteristics of all OMZswith respect to OXY, CORE and LOG all validate the CRIO criterion,which was chosen from the characteristics of the OMZ off Chile.However, in the future, and depending on the improvements inthe detection of O2, CRIO could be adapted for specific and regionalstudies and processes in the OMZs (e.g., canonical denitrification;sulfate-reduction and sulphide release). Moreover, oxygen mea-surements and CRIO do not account for microzone anoxia thatmight be associated with particles like marine snow in the low-oxygen water column.
The similarities among all the OMZs, characterized from CRIO,allow us to hypothesize that all OMZs are the consequences of sim-ilar dynamical (low ventilation) and biogeochemical (O2 consump-tion) processes. However, the marked differences between OMZsand the classical O2 minima suggest that, regionally, either differ-ent mechanisms or different intensity control each contractionand extent of an OMZ. The maintaining of the OMZ formed by threelayers (OXY, CORE, LOG), related to a large range of O2 concentra-tions, involves complex biogeochemical processes which should
focus the attention for future studies. Otherwise, the OMZ andNMZ reference states proposed in the present study could help toevaluate past and future variations in OMZs extent, and to under-stand the biogeochemical cycles and biological anomalies inducedby the OMZ formation.
5. Conclusion
The global ocean area and volume occupied by the most intenseOMZs (O2 < 20 lM) have been evaluated: 30.4 ± 3 millions of km2
and 102 ± 15 millions of km3, accounting for, respectively, 8% and7% of the global ocean. These results suggest that the extent ofthe OMZs was previously underestimated in the open ocean.
Horizontally, this study allowed to distinguish the permanentOMZs, despite seasonality changes (contraction; expansion) of10–15%, and the seasonal OMZs which completely disappear forseveral months during the year. The permanent OMZs are foundin the same four regions as those in which hypoxia and denitrifica-tion have been previously identified: ETNP, ESP, AS, BB. But, thepresent study also points out the formation of permanent OMZsin subtropical latitudes, such as the deep ESTNP, between 25�Nand 52�N, and very well dissociated from the well known ETNP.OMZs also formed seasonally in high latitudes: WBS (45–65�N;175–210�W) with a surface similar to that of the AS OMZ, whichappears mainly in winter, and in the GA (52–65�N; 120–175�W)which only disappears in summer. The seasonality of the OMZsappears more complex, with a vertical expansion often associatedwith an opposite horizontal contraction and CORE intensificationduring spring-summer, and is difficult to investigate from the cur-rently available global data.
Vertically, the OMZs, which are overall little oxygenated(�88 lM), show common characteristics including three layers:(i) an OXY: strong (�1.6 lM/m), four times more oxygenated(�65 lM) than the CORE, shallow (from 10–20 m depth) interfac-ing with the euphotic zone, and with the maximal annual mixedlayer depth; (ii) a CORE: intense (O2 < 20 lM), highly deficient inO2 (�15 lM), between 160 and 1080 m depth; (iii) a LOG: oneorder of magnitude thicker (�2580 m), less strong (�0.04 lM/m),and 35% more oxygenated (�100 lM) than for the OXY. The OMZs,localized in the EP, NI, WB and GA, and reaching O2 concentrationsdown to <1 lM in the CORE in the subsurface, are different fromthe relatively well-known ‘‘classical O2 minimum”, which is �50times more oxygenated and found in the intermediate waters(1000–1500 m) of all the oceans. The CORE of all OMZs occupiesa volume ten times smaller than the one occupied by the wholeOMZ, including OXY and LOG. OXY presents a similar thicknessto that of the CORE, �10% of the total OMZ thickness. LOG is oneorder of magnitude thicker (80%) than the CORE. This study pro-posed therefore a characterization of the vertical OMZs structurewith three layers, instead of considering the lowest O2 concentra-tions in the CORE only, as previously performed.
All OMZs are associated with NMZs (defined as NDEF > 10 lM),except the ESTNP OMZ and the LOZs in the eastern Atlantic. Theglobal NMZ here evaluated at 15 ± 1 millions km2 without includ-ing the Arctic NMZ, suggests that the global denitrification zonewas underestimated at least by a factor of 2 in the previous studies.Horizontally, because the global extent of the NMZs is three timessmaller than that of the OMZs, denitrification zones could alsounderestimate the OMZs area. Vertically, the NMZ estimate leadsto an underestimation of the extent by factors of �1.5 for the COREand �15 considering the total OMZ tickness. The reasons whydenitrification zones underestimate the OMZ extents are: (i) thedenitrification occurs mainly in a restricted volume compared tothe entire OMZ CORE volume (O2 < 20 lM); (ii) other biogeochem-ical OMZ-specific processes, especially linked to the nitrogen cycle,are not taken into account by the use of indirect indices
A. Paulmier, D. Ruiz-Pino / Progress in Oceanography 80 (2009) 113–128 127
(e.g., NDEF) for the detection of the denitrification. Consequently,the extents of the NMZs and OMZs suggest that the ocean couldlose more nitrogen than previously thought.
The most extended NMZs in the ETNP and ESP represent 52%and 28% of the global NMZ area, respectively, and the NMZ in theAS is the thickest (760 m). The ETNP and the ESP (off Chile andPeru) form the most intense NMZs (NDEFmax between 22 and27 lM), also corresponding to the most intense OMZ CORE (O2
min between 2 and 3 lM). For the seasonal WB and GA OMZs, thereare not enough data to evaluate their associated NMZ. On the otherhand, a polar NMZ was detected in the Arctic Ocean mainly on thelarge western continental margins associated with high denitrifica-tion in suboxic-anoxic sediments, whereas no Arctic OMZ was de-tected in the water column. NMZ extents are always lower thanthose of the OMZs, and the differences could be related to the avail-ability of O2: the more intense the OMZ is, the smaller is the differ-ence between the dimensions of the NMZ and of the OMZ. Thus,the ESTNP, BB and ESP near the equator, which are the most oxy-genated OMZs, have the most underestimated OMZs in volume(<50%), by the criterion of denitrification.
The OMZ extent and vertical structure, determined in the pres-ent study, could be used to evaluate past and future variations ofOMZs, linked to both climatic (temperature increase) and environ-mental (fertilization by nutrients) changes. To improve the estima-tion of the extent of the OMZ, it will be necessary to reduceuncertainties in vertical extent (about 10%) for all the OMZs,including the less known ESTNP OMZ. We recommend systematicsampling programs adapted to ultra-low O2 (<1 lM) for the CORE,with high resolution: vertically, 5–10 m or continuous (as withnew microsensors); horizontally, <1/4�. These recommendationsshould be taken into account in the new O2-measurements pro-jects (e.g., ARGO-Oxygen, recently proposed by Gruber et al.,2007; the European project Oxywatch), especially in the mostextensive and intense OMZs such as the ETNP. The first step to-wards new OMZ studies is to: (i) documentate the intensity, extentand seasonally changes in all the OMZs; (ii) elucidate the still un-known physical and biogeochemical mechanisms that form andmaintain intense and extensive OMZs in the modern ocean. Other-wise, all our efforts to predict OMZ extent and impact on ecosys-tems and biodiversity, using mathematical 3-D coupledcirculation and biogeochemical models, as a consequence ofanthropogenic fertilization and climate change, will be in vain.
6. Main acronyms
AS: Arabian Sea; BB: Bay of Bengal; BlS: Black Sea; BS: Baltic Sea;C: Carbon; CORE: OMZ core (O2 < 20 lM); CRIO: criterion on O2 tocharacterize the OMZ OXY, CORE and LOG; ENP/ESP: easternNorth/South Pacific; ESPC/ESPEq/ESPP: eastern South Pacific offChile/near the equator/off Peru; EP: eastern Pacific; ESTNP: easternsubtropical North Pacific; ETNP: eastern tropical North Pacific; GA:Gulf of Alaska; ‘‘isominox”/”isomaxndef”: depth of minimal O2
concentration (‘‘iso-mininimum of oxygen”)/maximal NDEF; LOG:lower O2 gradient; LOZ: low O2 zone (e.g., in the eastern Atlantic);N: Nitrogen; NI: northern Indian Ocean; NDEF: nitrate deficit(NO�3 ); NMZ: NDEF (>10 lM) maximum zone; OMZ: oxygen mini-mum zone; OXY: oxycline; PG; Persian Gulf; RS: Red Sea; SWACM:southwest African continental margin; WBS: western Bering Sea;WOA2005: World Ocean Atlas 2005; Ze/Zm: euphotic layer/maximalmixed-layer depth.
Acknowledgments
This study was supported by a French CNRS Ph.D. Fellowship toA. Paulmier and financial support was provided by IRONAGE (Euro-pean Union Program), the ECOS Sur program (French Ministry of
Foreign Affairs) and the University of Paris VI. We thank V. Garçonfor critical reading of an early manuscript version, C. Duarte, H.J.Minas and M. Graco for the successful discussions. Thanks to R.Griffiths for correcting the English, and C. Provost, L. Mortier, M.Crépon, MN Houssais and JM André, for helping and encouragingthis work.
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