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Oceanographic and Biological Effects of Shoaling of the Oxygen Minimum Zone

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Oceanographic and Biological Effects of Shoaling of the Oxygen Minimum Zone MA05CH17-Gilly ARI 9 November 2012 14:53 Oceanographic and Biological Effects of Shoaling of the Oxygen Minimum Zone William F. Gilly,1 J. Michael Beman,2 Steven Y. Litvin,1 and Bruce H. Robison3 1Hopkins Marine Station, Stanford University, Pacific Grove, California 93950; email: [email protected], [email protected] 2School of Natural Sciences and Sierra Nevada Research Institute, University of California, Merced, California 95343; email: [email protected] 3Monterey Bay Aquarium Research Institute, Moss Landing, California 95039; email: [email protected] Annu. Rev. Mar. Sci. 2013. 5:393–420 Keywords First published online as a Review in Advance on hypoxia, ecology, oceans, microbial, mesopelagic, fisheries September 17, 2012 The Annual Review of Marine Science is online at Abstract marine.annualreviews.org Long-term declines in oxygen concentrations are evident throughout much This article’s doi: of the ocean interior and are particularly acute in midwater oxygen mini- 10.1146/annurev-marine-120710-100849 mum zones (OMZs). These regions are defined by extremely low oxygen Copyright c 2013 by Annual Reviews. < μ −1 Annu. Rev. Marine. Sci. 2013.5:393-420. Downloaded from www.annualreviews.org concentrations ( 20–45 mol kg ), cover wide expanses of the ocean, and All rights reserved are associated with productive oceanic and coastal regions. OMZs have ex- panded over the past 50 years, and this expansion is predicted to continue as the climate warms worldwide. Shoaling of the upper boundaries of the by Stanford University - Hopkins Marine Station SEPARATE ACCOUNT on 01/28/14. For personal use only. OMZs accompanies OMZ expansion, and decreased oxygen at shallower depths can affect all marine organisms through multiple direct and indirect mechanisms. Effects include altered microbial processes that produce and consume key nutrients and gases, changes in predator-prey dynamics, and shifts in the abundance and accessibility of commercially fished species. Al- though many species will be negatively affected by these effects, others may expand their range or exploit new niches. OMZ shoaling is thus likely to have major and far-reaching consequences. 393 MA05CH17-Gilly ARI 9 November 2012 14:53 INTRODUCTION Oxygen plays a key role in structuring marine ecosystems and controls the spatial and temporal Euphotic zone: the distribution of essentially all marine organisms, from microbes to zooplankton, squid, fish, and depth range in the (indirectly) marine mammals. Along with light, temperature, salinity, and dissolved nutrients, water column where the concentration of dissolved oxygen in the ocean varies greatly with depth. Sunlight heats the sufficient light epipelagic (surface) layer of the ocean and drives photosynthesis by phytoplankton (primary pro- penetrates to support photosynthesis by duction), leading to thermal stratification and the export of production from the euphotic zone phytoplankton; vision to depth. Below the euphotic zone, microbial respiration consumes oxygen, causing oxygen to by midwater animals decline. However, in certain areas where surface production is elevated and the deep circulation generally extends to of oxygen-rich water derived from polar regions is sluggish, microbial respiration consumes sub- greater depths stantial quantities of oxygen that are only slowly replenished, forming steady-state low-oxygen Microbial zones in the water column. In such areas, oxygen falls to very low values and then rises again as respiration: depth increases; these areas are called oxygen minimum zones (OMZs) (Wyrtki 1962, Fiedler & consumption of organic matter and Talley 2006, Pennington et al. 2007, Karstensen et al. 2008, Fuenzalida et al. 2009, Paulmier & oxygen and release of Ruiz-Pino 2009, Keeling et al. 2010, Stramma et al. 2010). CO2 by microorganisms, including photosynthetic OMZs: WHAT ARE THEY? phytoplankton that An all-encompassing definition of an OMZ based on absolute oxygen concentrations is not real- respire at night istic, because no single oxygen concentration defines a universal level of hypoxic stress for marine Oxygen minimum organisms (Seibel 2011). OMZs in the eastern Pacific, the primary focus of this review, are char- zone (OMZ): a <∼ midwater depth range acterized by an oxygen saturation level that is 10% of that at the sea surface. This corresponds −1 −1 −1 where the oxygen to an oxygen concentration of <20 μmol kg (0.5 ml liter or 0.7 mg liter ) (Levin 2003b, concentration is Helly & Levin 2004, Paulmier & Ruiz-Pino 2009), a value close to that where anaerobic microbial −1 <20 μmol kg in the processes become dominant (5–20 μmol kg−1) (Karstensen et al. 2008, A.F. Hofmann et al. 2011). Pacific and Indian Oxygen levels this low are severely hypoxic for most familiar large organisms, and metazoans Oceans or − <45 μmol kg 1 in the inhabiting such strong OMZs show a variety of adaptations to hypoxia (Childress 1995, Childress Atlantic Ocean & Seibel 1998, Drazen & Seibel 2007, Seibel 2011). Anaerobic microbial Although this definition of an OMZ based on microbial activity is nonarbitrary and useful in the processes: reactions eastern Pacific and Indian Oceans (Figure 1), it is not universally applicable. Well-defined OMZs using oxidized exist in the eastern Atlantic (Stramma et al. 2008a,b, 2010), but the oxygen concentration in the compounds other than core of the strongest Atlantic OMZ is >20 μmol kg−1, which is significantly higher than those in O2 (e.g., nitrate or the Pacific and Indian Ocean OMZs, where the oxygen level can approach zero (Karstensen et al. sulfate) as an electron acceptor, allowing 2008, Canfield et al. 2010). This complicates identifying a specific oxygen boundary for Atlantic < μ −1 Annu. Rev. Marine. Sci. 2013.5:393-420. Downloaded from www.annualreviews.org microbes to persist in OMZs, but a concentration of 45 mol kg has been proposed to define OMZs in this region the absence of O2 (Karstensen et al. 2008). Oxygen limited zone These definitions of an OMZ are consistent with physiological data indicating that an oxygen (OLZ): the region concentration range of 60–120 μmol kg−1 is seriously hypoxic for many marine organisms by Stanford University - Hopkins Marine Station SEPARATE ACCOUNT on 01/28/14. For personal use only. immediately above or (Diaz & Rosenberg 1995, Miller et al. 2002, Vaquer-Sunyer & Duarte 2008; tolerances of below an OMZ with an OMZ-associated species are discussed in Ekau et al. 2010). The lower end of this range leads to oxygen concentration − of <60 μmol kg 1 in hypoxic stress for many marine organisms (Seibel 2011) and has often been used to define hypoxic the Pacific and Indian habitats at depth (Whitney et al. 2007, Bograd et al. 2008, Ekau et al. 2010, Keeling et al. 2010). Oceans or For the Pacific and Indian Oceans, we therefore use an oxygen concentration of <60 μmol kg−1 −1 <90 μmol kg in the to define the hypoxic regions above and below an OMZ’s vertical boundaries as oxygen limited Atlantic Ocean zones (OLZs) (Figure 2a) (Gilly et al. 2012). These regions are sometimes called oxyclines, but this term is obviously imprecise. An oxygen concentration of <90 μmol kg−1 has been proposed to define analogous OLZs in the eastern Atlantic Ocean (Karstensen et al. 2008). 394 Gilly et al. MA05CH17-Gilly ARI 9 November 2012 14:53 90° N 20 Integrated dissolved oxygen dissolved Integrated a 200 to 700 m (mol from 60° N 16 30° N 12 0° Latitude 8 30° S 4 –2 60° S ) 90° S 0 90° N 1,500 b 60° N 1,250 Depth of 20 μmol liter dissolved oxygen (m) oxygen dissolved 30° N 1,000 0° 750 Latitude 30° S 500 –1 60° S 250 90° S 0 90° N 1,500 c 60° N 1,250 Depth of 60 μmol liter dissolved oxygen (m) oxygen dissolved 30° N 1,000 0° 750 Latitude 30° S 500 –1 60° S 250 Annu. Rev. Marine. Sci. 2013.5:393-420. Downloaded from www.annualreviews.org 90° S 0 90° E 180° 90° W 0° Longitude by Stanford University - Hopkins Marine Station SEPARATE ACCOUNT on 01/28/14. For personal use only. Figure 1 Oceanic oxygen minimum zones (OMZs). (a) Integrated dissolved oxygen concentrations from 200 to 700 m depth in the water column (Garcia et al. 2006). Purple areas are regions with strong OMZs. Only the Pacific − − and Indian Oceans have areas with values of <2molm 2.(b)Depthsofthe20μmol liter 1 oxygen isopleths that define the upper boundaries of the strong OMZs in the eastern Pacific and Indian Oceans. Oxygen − − concentrations in the gray areas are >20 μmol liter 1.(c)Depthsofthe60μmol liter 1 oxygen isopleths that we use to define the upper boundaries of the oxygen limited zones (OLZs), hypoxic areas above the − − OMZs proper. Oxygen concentrations in the gray areas are >60 μmol liter 1.Theunitsofμmol liter 1 and μmol kg−1 are not the same, but they are interchangeable for our purposes here. www.annualreviews.org • OMZ Shoaling and Changing Seas 395 MA05CH17-Gilly ARI 9 November 2012 14:53 a b Oxygen concentration (µmol kg–1) C-cycling processes N-cycling processes S-cycling processes 6020 100 150 200 250 0 Euphotic Oxygenic photosynthesis N2 xation zone CO2 + H2O Organic C+ O2 N2 NH3 50 Aerobic respiration Nitrication S oxidation – – Organic C + O2 CO2 + H2O NH3 + O2 NO2 NO3 Reduced S + O2 Oxidized S 100 OLZ N2O N2O Depth (m) Chemoautotrophic 150 Denitrication denitrication – – Organic C + NO3 CO2 + N2 H2S + NO3 Oxidized S + N2 OMZ N2O N2O 200 Anammox Sulfate reduction – 2– NH3 + NO2 N2 + H2O Organic C + SO4 CO2 + H2S N2O 250 Figure 2 Microbial biogeochemical processes active in oxygen minimum zones (OMZs) and the oxygenated ocean. (a) Characteristic depth profile for dissolved oxygen in the eastern tropical North Pacific (Beman et al. 2012), indicating the depths of the euphotic zone ( yellow), oxygen limited zone (OLZ; light gray), and OMZ (dark gray) as defined in this review.
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