Oxygen minimum zones (OMZs) in the modern ocean
Introduction
The interest in oxygen minimum zones (OMZs), characterized herein as O2-deficient layers in the ocean water column, is quite recent, since the appearance of the name “OMZ” in Cline and Richards (1972). OMZs correspond to subsurface oceanic zones (e.g., at 50–100 m depth in the Arabian Sea; Morrison et al., 1999) and reaching ultra-low values of O2 concentration (e.g. <1 μM; 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 at intermediate 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.
OMZs have been mainly known for playing an essential role in the global nitrogen cycle, in which various chemical species, according to their degree of oxidation (e.g. ammonium, ; nitrite, ; nitrate, ; nitrous oxide, N2O; dinitrogen, N2), and different bacterial processes intervene. Under oxic conditions, but also at the upper boundary (oxycline) of an OMZ, nitrification transforms into . But OMZs are especially associated with denitrification, which is a bacterial process occurring only in O2-deficient regions (e.g., Codispoti et al., 2001). Denitrification converts , one of the main limiting nutrients in the ocean, into gaseous nitrogen (N as, for example, N2O, N2) which is lost to the atmosphere and contributes to the oceanic nitrate deficit (N/P ≈ 14.7; e.g., Tyrrell, 1999). However, recently, an unknown process in the ocean has been observed, first in sediments and then in the water column in the OMZs (e.g., Kuypers et al., 2003): the anaerobic oxidation of using (anammox); this imposes a complete revision of the global nitrogen cycle (e.g., Arrigo, 2005). OMZs are also involved in the cycle of very important climatic gases: (i) production of ∼50% of the oceanic N2O (e.g., Bange et al., 1996); (ii) production of H2 S (e.g., Dugdale et al., 1977) and CH4 (e.g., Cicerone and Oremland, 1988), episodically or for OMZs in contact with sediments; (iii) limitation of atmospheric CO2 sequestration by the ocean: directly as an end-product of remineralization (Paulmier et al., 2006) or indirectly through limitation of total primary production due to the N loss (see hypothesis of Falkowski, 1997); (iv) potential DMS consumption due to higher bacterial activity (Kiene and Bates, 1990). Chemically, OMZs are associated with acidification (low pH ≈ 7.5 SWS; Paulmier, 2005), and reduced conditions (Richards, 1965) favoring reduced chemical species (e.g., Fe(II) or Cu(I) potentially stimulating photosynthesis or N2O production).
OMZs have also increased interest in biological and ecosystem studies. Because of similarities between Archean bacteria and those living in the OMZs (Zumft, 1997), OMZs could be considered as analogues of the primitive anoxic ocean in which life is widely thought to have first appeared. Transitions from high to low (the appearance of OMZs) oxygenation periods could stimulate biodiversity on a paleoclimatic scale (Rogers, 2000). OMZs can be a refuge for organisms specifically adapted to low O2 concentration (e.g., giant Thioploca bacteria; Levin, 2002) from predation or competition with other species, and the lower OMZ boundary can even be among the richest habitats for the megafauna of the ocean. As a respiratory barrier, 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 Anoxic Events (OAEs) have been associated with massive species extinction (e.g. during the Mid-Cretaceous). In the present, episodic anoxic events associated with eutrophicated waters are also inducing massive abnormal fish mortality (e.g., Chan et al., 2008).
The intensity of all OMZ’s perturbations and their potential feedback to climate and the marine ecosystem would depend on the OMZs extent. This extent would vary in response to climatic changes (lower ventilation due to stratification, and decreased O2 solubility) and natural or anthropogenic fertilization (increased remineralization) 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 and contracted in warm (interglacial) and cold (glacial) periods, respectively (e.g., Cannariato and Kennett, 1999). Under present-day conditions, OMZs would increase or intensify, according to observations in recent decades (e.g., Stramma et al., 2008). But evaluations or predictions of OMZs variation over paleoclimatic periods, since the anthropocene era or in the future, cannot be validated without a reference state, and the report of all the existing OMZs detected in the modern ocean taking into account improvements in O2-measurement techniques.
Despite the important role of OMZs in understanding primitive marine life and chemistry, as well as in the carbon (C) and nitrogen (N) cycles, little knowledge has been obtained on the extent and vertical structure of these oceanic “curiosities”. This is mainly due to the following difficulties: (i) few available O2 data obtained with a low enough detection limit (<1 μM) and accuracy (<2 μM), owing to the present limitations in the sampling and analysis techniques linked to the low O2 concentration; (ii) the choice of a unique criterion for all OMZs, since the nature of this criterion often depends on research interest (e.g., specific low-O2 biogeochemistry process studies have to take into account an O2 concentration lower than 20 μM, but the influence of physical processes do not make it necessary to include suboxic and anoxic conditions); (iii) the criteria could be different for each OMZ region: for example, the OMZs in the Northeastern Atlantic ocean is excluded when a threshold of 20 μM is used (Helly and Levin, 2004). Different terms and thresholds have been used to described the overall low O2 conditions. Suboxia has been mainly defined by biologists and biogeochemists as a transition layer from O2- to -respiration, with thresholds between ∼0.7 μM (e.g., Yakusev and Neretin, 1997) and 20 μM (e.g., Helly and Levin, 2004). Hypoxia implies O2 conditions under which macro-organisms cannot live: ∼8 μM for Kamykowski and Zentara (1990), but up to 40 μM depending on the species considered, such as anchovy (e.g., Gray et al., 2002). Dysoxia (O2 < 4 μM) and microxia (O2 < 1 μM; Levin, 2002) are associated with a sharp O2 transition for the large organisms, such as fishes. Anoxia (O2 < 0.1 μM; Oguz et al., 2000) is defined by transition from NO3-respiration to sulphate-reduction.
The first global study providing information on where water column OMZs can be located is that of Kamykowski and Zentara (1990) who produced maps of the distribution of hypoxia (O2 < 8 μM) and of denitrification (Nitrate DEFicit or NDEF > 10 μM): ENP (Eastern North Pacific), ESP (Eastern South Pacific), AS (Arabian Sea) and BB (Bay of Bengal; see Fig. 1a). Without having a known evaluation of an OMZ’s surface and vertical structure, Codispoti et al. (2001) concluded that the volume of suboxic zones could reach ∼0.1% of the oceanic volume. OMZ areas have been considered to be similar to those of denitrification in several regional studies: 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 criteria for each OMZ: NDEF > 10 μM (AS); secondary subsurface peak (ESP); O2 < 5 μM (ENP). But from a qualitative comparison of hypoxia and denitrification maps, Kamykowski and Zentara (1990) concluded that the extent of the denitrification zone would be much less than the extent of the OMZ. Such a difference shows that the denitrification criterion could not be adapted to evaluating the size of the whole O2-deficit zone. To validate this hypothesis, it is necessary to evaluate OMZs independently of the extent of the denitrification zone. Note also that the surface of OMZs that is in contact with sediments (1372 × 106 km2; Helly and Levin, 2004) would be an order of magnitude lower than the global denitrification zone and the associated water-column OMZ surfaces.
Estimations of the extent of OMZs for biogeochemical studies are scarce and/or local (e.g., Morrison et al., 1999). Recently, the quantification of OMZs in the open ocean has been proposed by Karstensen et al. (2008). In the present study, three O2 thresholds were used (the suboxic level of 4.5 μmol/kg, a more stringent 45 μmol/kg and a more relaxed level of 90 μmol/kg), and the analyses were focused on the tropical Atlantic and Pacific Oceans. The OMZ volumes thus evaluated were of 0.461, 18.6 and 38.3 × 106 km3 for each proposed O2 threshold, respectively. Although not focused on the OMZs in the Indian Ocean, Karstensen et al. (2008) proposed an estimation of the vertical extent for the OMZ in the Arabian Sea of 550 m, i.e. about twice as small as the local evaluation by Morrison et al. (1999). Why another evaluation of OMZ extent and volume? Because our focus is on defining an OMZ structure and extent which allows us to take into account specific biogeochemical processes, such as denitrification or anammox, associated with low O2. The evaluation and criteria proposed by Karstensen and coauthors are more adapted to the analysis of the dynamical processes responsible for the formation of an OMZ, though excluding the formation of OMZs in the Indian Ocean, where probably the most intense denitrification and nitrogen loss occur, and such as we will see here, do not include OMZs at a high subtropical latitude. It was shown from an analysis of the ESP OMZ off Chile (Paulmier et al., 2006) that the existence of three different layers has to be taken into account to evaluate the entire OMZ structure: the oxycline (upper O2 gradient, ∼5 times more intense than in the oxygenated ocean); the core (O2 < 20 μM); the lower O2 gradient. Indeed, the oxycline is considered as the OMZ engine, where the most intense remineralization occurs, leading to the OMZ’s intensification, and where a specific denitrification and nitrification coupling (e.g., Brandes et al., 2007) could also occur with O2 > 20 μM. OMZ core, specific to anaerobic processes as canonical (classical anaerobic) denitrification, and the lower O2 gradient, where nitrification is a main process, could play an important role in the nitrogen cycling in the OMZ (e.g., Anderson et al., 1982). Thus, to consider the specific biogeochemical processes, it is necessary to include 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 denitrification criteria are or are not adapted to the evaluation of the extent of an OMZ, it is necessary to determine simultaneously the structure and extent of OMZ and the denitrification zones.
Hence, from the same O2 criterion and comparison with the criteria for denitrification, the main and most intense OMZs in the open ocean are identified and characterized quantitatively (horizontally and vertically). The permanence and potential seasonality of the OMZs will be analyzed. However, OMZs formed over the continental shelf (such as the Benguela OMZ) and in semi-enclosed seas (such as the Black Sea) or over deep trenches (e.g. Gulf of Cariaco, Venezuela) reaching the level of anoxia will not be addressed in this study.
Section snippets
Methodology
To characterize and determine the surface and volume of an OMZ, the CRIO criterion on O2, adapted to take into account the entire vertical thickness of an OMZ, and compared with the denitrification criteria, was applied to the WOA2005 (World Ocean Atlas, 2005) data.
Results
The results presented concern the extents of the OMZs and the NMZs.
Discussion
OMZs and NMZs characterized in this study were compared between themselves, and with the classical O2 minimum and previous evaluations. Then, the choice of a criterion to take into account the entire OMZ volume associated with OMZs is discussed.
Conclusion
The global ocean area and volume occupied by the most intense OMZs (O2 < 20 μM) have been evaluated: 30.4 ± 3 millions of km2 and 102 ± 15 millions of km3, accounting for, respectively, 8% and 7% of the global ocean. These results suggest that the extent of the OMZs was previously underestimated in the open ocean.
Horizontally, this study allowed to distinguish the permanent OMZs, despite seasonality changes (contraction; expansion) of 10–15%, and the seasonal OMZs which completely disappear for
Main acronyms
AS: Arabian Sea; BB: Bay of Bengal; BlS: Black Sea; BS: Baltic Sea; C: Carbon; CORE: OMZ core (O2 < 20 μM); CRIO: criterion on O2 to characterize the OMZ OXY, CORE and LOG; ENP/ESP: eastern North/South Pacific; ESPC/ESPEq/ESPP: eastern South Pacific off Chile/near the equator/off Peru; EP: eastern Pacific; ESTNP: eastern subtropical North Pacific; ETNP: eastern tropical North Pacific; GA: Gulf of Alaska; “isominox”/”isomaxndef”: depth of minimal O2 concentration (“iso-mininimum of oxygen”)/maximal
Acknowledgments
This study was supported by a French CNRS Ph.D. Fellowship to A. Paulmier and financial support was provided by IRONAGE (European Union Program), the ECOS Sur program (French Ministry of Foreign Affairs) and the University of Paris VI. We thank V. Garçon for 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
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