Deep Sea Research Part I: Oceanographic Research Papers
Hypoxia by degrees: Establishing definitions for a changing ocean
Highlights
► We propose a unified set of thresholds for “hypoxia” using consistent units. ► Partial O2 pressure is the limiting variable: thresholds should be reported as pO2. ► No confusion of coastal hypoxia and O2 minimum zones: different time scales apply. ► Upwelling from O2 minimum zones can cause coastal hypoxia: we give hot spots.
Introduction
The term “dead zone” is now widely used in the media, and often by scientists to describe a situation where dissolved oxygen levels are so low as to pose a threat to marine life but the term appears to have no specific or universal meaning. It appears to be of recent origin as traditional texts (e.g. Sverdrup et al., 1942, Redfield et al., 1963, Richards, 1965, Riley and Skirrow, 1965, Riley and Skirrow, 1975) make no use of this wording and the word “dead” is informally assumed to be not absolute. For example the widely described dead zone off the Mississippi delta (e.g. Turner et al., 2008) is not absolutely dead to aerobic life; the nomenclature refers primarily to the important impact on the local shrimp fishery (Lumcon, 2010). Furthermore, various other oxygen thresholds are presented in a bewildering set of units and the resulting confusion impedes useful discussion of genuine limits of various kinds, and inhibits adequate documentation and reporting of significant changes that are now taking place such as apparent long term declines in oceanic oxygen concentrations (Chen et al., 1999, Nakanowatari et al., 2007, Jenkins, 2008, Stramma et al., 2008, Shaffer et al., 2009) associated with ocean warming (Lyman et al., 2010).
A more structured yet not unambiguous approach for a characterization of low oxygen zones is the use of the terms “hypoxia”, “suboxia”, and “anoxia”. Hypoxia was originally meant to describe internal stress on an animal (e.g. Piiper, 1982) but was quickly applied to describe the external ocean medium. Many thresholds for hypoxia in differing units have been used, the most prominent one being 2 mgO2/l () (e.g. Gray et al., 2002). Ocean chemical definitions have traditionally used the term “suboxic” (Sillen, 1965) for the situation where dissolved oxygen levels are so low that microbes begin to turn to nitrate as an alternate electron acceptor and a cascade of redox reactions begins to appear (Kamykowski and Zentara, 1990, Rue et al., 1997). The suboxic limit is typically set at around and it represents a quite strict definition; the threshold of set by Kamykowski and Zentara (1990) was chosen to represent regions where significant nitrate loss was already large and suboxic microbial change is already well underway. However, “suboxic” recently has also been used to define thresholds in connection with macroorganisms (e.g. Shaffer et al., 2009). Even the seemingly unambiguous term “anoxia” is sometimes defined not as the true zero dissolved oxygen state but as 0.2 mlO2/l (Gooday et al., 2009a). And even under true zero oxygen and sulfide rich conditions some forms of multicellular animals have evolved (Danovaro et al., 2010). There are several problems with definitions based simply upon a concentration limit applied ocean wide with the principal ones being that the same limit appears to be applied over a range of temperature spanning some 30 °C from the tropics to the polar regions, and over a depth range spanning thousands of meters.
Today, dissolved oxygen dead zone or hypoxia thresholds such as the Mississippi delta dead zone threshold of 2 mgO2/l () (Turner et al., 2008), originally defined for species communities in comparatively warm, near shore ecosystems experiencing seasonal oxygen depletion (Gray et al., 2002, Diaz and Rosenberg, 2008, Turner et al., 2008, Gooday et al., 2009a, Kemp et al., 2009, Levin et al., 2009, Middelburg and Levin, 2009, Zhang et al., 2010) are increasingly applied to open ocean permanent oxygen minimum zones (e.g. Shaffer et al., 2009). Those permanent oxygen minimum zones, particularly the Eastern North Pacific and the Indian Ocean, as classically described by Wyrtki (1962), Kamykowski and Zentara (1990), Olson et al. (1993), are inhabited by species communities adapted to low oxygen concentrations (e.g. Childress and Seibel, 1998, Levin, 2003, Diaz and Rosenberg, 2008; Gooday et al., 2009a, Gooday et al., 2009b, Gooday et al., 2010; Levin et al., 2009) and coastal thresholds have no equivalent meaning. For example the model study of Shaffer et al. (2009) correctly concludes that by the year 2500 up to 61% of the total ocean volume will be “hypoxic”, as defined by here, compared to 9.1% for the present ocean ( Codispoti, 2010). But there is no widespread knowledge of what the hypoxia definition implies for species communities spanning a wide range of temperature and depth. For example Seibel et al. (1999) report thriving vampire squid populations in the lowest oxygen levels encountered in the oxygen minimum zone off California (, e.g. McClatchie et al., 2010), while other authors claim even the conventional hypoxia threshold of 2 mgO2/l () is below the empirical sublethal and lethal O2 thresholds for half of their tested species (Vaquer-Sunyer and Duarte, 2008).
Two basic mechanisms causing coastal hypoxia are eutrophication due to land and river based nutrient input leading to local microbial oxygen consumption (e.g. Gulf of Mexico, Turner et al., 2008, Hogue, 2010, Lumcon, 2010), and upwelling of oxygen depleted, nutrient rich water from bathyal oxygen minimum zones where deep microbial oxygen consumption occurs (e.g. Oregon coast, Grantham et al., 2004, Chan et al., 2008, Gewin, 2010). While horizontal advection of low oxygen waters should not be neglected (e.g. Bograd et al., 2008, Connolly et al., 2010, Rabalais et al., 2010), here we are primarily concerned with upwelling from the vast reservoir of low oxygen waters in oxygen minimum zones.
The oxygen content of water masses usually is characterized by dissolved oxygen concentration units since these are conservative with respect to the temperature and salinity and can be used for mass balances, mixing calculations, and numerical modeling. This leads to oxygen thresholds also being reported in dissolved oxygen concentration units. However, animals depend on gas exchange across membranes and tissues for critical physiological processes such as respiration and also for controlling gas exchange with the swim bladder of fishes (e.g. Enns et al., 1965, Childress and Seibel, 1998, Pelster and Burggren, 1996, Piiper, 1982); the appropriate thermodynamic property for this is the gas fugacity which is readily approximated by the partial pressure. Experimental work on respiration of marine animals must thus essentially report pO2 as the critical variable (e.g. Seibel, 2011). Since the partial pressure of a gas is a function of temperature, pressure (Enns et al., 1965), and salinity, thresholds reported as concentration units are not universally applicable but only valid for systems with particular temperature, pressure and salinity. Oxygen thresholds in terms of partial pressure, however, are universally applicable.1
In this paper we take steps towards overcoming three of the most fundamental shortcomings of low oxygen science today: (1) we plead for a consistent use of terminology and units by comparing and interrelating existing oxygen thresholds from the literature. (2) We restate that partial pressure of O2 is required for defining organism needs and stresses and we propose a scale for definition of hypoxic events based on partial pressure. (3) We establish the connection between bathyal oxygen minimum zones and coastal hypoxia by examining how close various coastal ocean regions (without enclosed seas) are, on a yearly averaged basis, to experience significant negative impacts by upwelling-induced hypoxia.
Section snippets
Oxygen concentration ([O2]) data
Oxygen concentration data2 in mlO2/l units from the Ocean Data View version of the global oxygen climatology given in the World Ocean Atlas 2009 (WOA09 Garcia et al., 2010) have been used as primary data source throughout this paper unless
pO2 as function of temperature, pressure, and salinity
Fig. 1 illustrates the dependency of oxygen partial pressure on temperature T, salinity S, and hydrostatic pressure P. For a given oxygen concentration of , pO2 increases from at the surface to 100 matm at depth if the temperature remains constant at 10 °C. At depth, pO2 would increase from 70 matm to 90 matm when temperature was to rise from 4 °C to 20 °C (left panel of Fig. 1). The effect of salinity S on pO2 is less pronounced (right panel of Fig. 1).
Categories of “hypoxia” based on oxygen partial pressure
Contemporary
The need for a common language
Without a common language, science is hard if not impossible to communicate either to other scientists or to the general public. Especially when scientific results and definitions are the basis for policies, regulations, and resource management decisions, inconsistent language can lead to misinterpretations with possible unfortunate consequences: oxygen levels that constitute a “dead zone” in one region of the ocean are the norm in others, with the distinction not always clear, possibly
Conclusions
Within the field low oxygen research, widely different thresholds with different units are used. A unified set of thresholds and a common language, as proposed here, will greatly benefit the field.
Ultimately limiting oxic respiration is the gradient in oxygen partial pressure pO2. Therefore, and due to the strong dependency of pO2 on temperature and hydrostatic pressure, any low oxygen threshold describing effects on animals should be reported as partial pressure not as concentration. Partial
Acknowledgments
This work was supported by a grant to the Monterey Bay Aquarium Research Institute from the David & Lucile Packard Foundation.
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