“Hypoxia,” a word used to describe oxygen deficiency, first came into use in the medical field during studies of metabolic function in the 1940s. Hypoxia was seen as something occurring within the body of a human or animal that was not getting enough oxygen for normal function. During the 1970s, “hypoxia” also came to be widely used to describe bodies of water so depleted of oxygen that they were harming or even killing the aquatic species that lived there.

When discussing specific waterways, many researchers adopted a standard definition of hypoxia: a dissolved oxygen concentration of 2 milligrams per liter or less. This level was chosen for its observed effects on fish. But extensive research over the past five decades has shown that the effects of low oxygen vary greatly by species and local environmental conditions. Now, new definitions of hypoxia are emerging, and some researchers have stopped using the term altogether when referring to waterways.

The origins

The word “hypoxia” derives from the Greek “hypo,” meaning low, and “oxia,” as related to oxygen. A French scientist, Jean-Paul Richalet, traced the first use of the word in the United States to the year 1940, when it was adopted to describe low-oxygen conditions in human cardiology and anesthesiology. “Hypoxia” came to be preferred over varying degrees of “anoxia” — which literally means without any oxygen.

“The clinical distinction between anoxia (a life-threatening condition) and hypoxia (a condition where defense mechanisms can restore vital functions) was clearly defined by Carl Wiggers and Ralph Waters in 1941 and 1944, respectively,” according to Richalet. “However, ‘anoxia’ continued to be widely used in the 40s and 50s.

“There is no single defined concentration at which marine, coastal or estuarine waters become hypoxic to the resident organisms, nor is there consistency in units of oxygen used to express hypoxia.”

“The frequent use of expressions such as “progressive anoxia” or “moderate anoxia” suggests that scientists used “anoxia” with the meaning of “hypoxia,” not considering the prefix ‘a-’ as a total absence of oxygen,” he continued. “Finally, hypoxia took the lead in the ’60s with the development of cell biology and high-altitude physiology and medicine.”

While the word “hypoxia” was coming into general use within the medical field, marine biologists were using the term to describe low-oxygen conditions and its effects on all sorts of animals. In laboratory studies, researchers exposed various marine creatures to low-oxygen waters to observe the response. One common measure of severity, called LC50, describes the “lethal concentration” of oxygen (referring to a lethal lack of oxygen) in water that kills 50 percent of the test subjects.

Researchers recognized the importance of various behavioral and physiological changes taking place at reduced oxygen levels — generally well above levels that killed fish, shellfish or other creatures being studied. They also acknowledged that even the most sophisticated lab experiments bore only a slight resemblance to the real world, in which animals can move or otherwise respond to constantly changing conditions in the water.

An elusive number

Coming up with reliable numbers for low-oxygen effects on marine life remained an elusive challenge, as two Oregon State University researchers, Peter Doudoroff and Dean Shumway, reported in 1970 in a United Nations technical report.

“One does not need to study the literature very long to become convinced that there is indeed little agreement of reported findings,” they wrote. “Minimum tolerable or ‘threshold’ levels of O2 reported by some investigators are several times greater than those reported by others for the same fish species, tested at about the same temperatures.

“Fish have been said by some to be capable and by others to be quite incapable of prompt detection and avoidance of low O2 concentrations,” they said. “Reduction of O2 sometimes has been said to depress activity and sometimes to cause increases of the activity of fish… The reasons for these apparent contradictions have not been adequately explained.”

The researchers reported on multiple studies that examined the effects of exposing fish to low-oxygen waters. They produced evidence showing that stressful — but not lethal — levels of oxygen can produce “chronic hypoxia” and eventual death through a “physiological disturbance that is different from the cause of death at rapidly lethal O2 levels,” they said. Deadly levels of oxygen, they added, produced “acute hypoxia,” in fish, keeping with the definition of hypoxia as a physiological condition.

Massive die-offs of Dungeness crab off the Pacific Northwest Coast have been attributed to dangerously low oxygen levels. Once dead, the aquatic crabs often wash up on beaches, as seen here on Kalaloch Beach on June 14, 2022. Jenny Waddell/NOAA

Meanwhile, concerns were growing through the 1970s and ’80s about the deteriorating condition of waterbodies throughout the United States. In 1985, the first “Nationwide Survey of Oxygen Depletion and Eutrophication in Coastal and Estuarine Waters” borrowed the term “hypoxia” from medicine and cellular biology to describe low-oxygen conditions found in natural waterways.

The authors did not define an oxygen level that would constitute hypoxia, but they used that term in reference to areas within waterways where people had observed and measured low-oxygen problems. They concluded that 38 percent of the nation’s major estuaries were experiencing hypoxia, referring in some cases to violations of locally established water-quality criteria, such as 4 milligrams/liter.

The survey specifically identified waterways of concern throughout the United States, including Budd Inlet in southern Puget Sound, listed as a “priority hypoxic area.” The report called out fish kills and oxygen levels as low as 1 mg/l in the inlet. Two other Puget Sound areas, Port Susan near Whidbey Island and Lynch Cove in southern Hood Canal, were declared “potential hypoxic areas.”

Algal blooms like the red-brown one seen here in Budd Inlet in September 2018 can contribute to low-oxygen waters. WA Department of Ecology

By 1986, multiple researchers, including Maurice Renaud of NOAA’s Southwest Fisheries Science Center, were using the precise number 2 mg/l to describe “hypoxic” conditions in the Gulf of Mexicoa, with various effects noted at this oxygen concentration. A few other researchers chose other hypoxic levels for their studies, such as 2.5 mg/l or sometimes higher.

A wide range of levels

In 1992, NOAA’s Office of Ocean Resources Conservation and Assessment (ORCA) launched a new program to better assess and compare the condition of estuaries nationwide, first collecting information in separate reports from five regions and then compiling a single national report. Eight parameters related to water quality were chosen for data gathering. To rank each parameter, specific thresholds were chosen. In the case of oxygen, “anoxia” was defined as 0 mg/l, “hypoxia” was between 0 and 2 mg/l, and “biological stress” was between 2 and 5 mg/l.

“The ranges were determined from nationwide data and from discussions with eutrophication experts,” states the first report from the South Atlantic Region. “The thresholds used to classify ranges are designed to distinguish conditions among estuaries on a national basis and may not distinguish among estuaries within a region.”

Concerns about low-oxygen conditions continued to grow for waterways throughout the country, as researchers reported an expansion of low-oxygen conditions in various waterways, while a new term, “dead zones,” was being bandied about in newspapers and eventually adopted in scientific and government reports. In 1998, Congress passed the Harmful Algal Bloom and Hypoxia Research and Control Act, which called for increasing research on hypoxic conditions. The reports generally stuck with 2 mg/l as the definition of hypoxia for the sake of comparing waterways nationwide.

Neither the term “hypoxia” nor the use of 2 mg/l as a universal threshold came about without objections. In 1991, Richard Tyson and Tom Pearson with the Geological Society of London proposed new terminology in a publication that sparked discussion.

“Physiologists have long used the term ‘hypoxia’ to describe conditions or responses produced by stressful levels of oxygen deficiency,” they wrote. “Its application to natural oxygen-deficient environments began to be common in the late 1970s, especially by those working in the Gulf of Mexico, and it is now in widespread use by marine biologists and ecologists…

“The term ‘hypoxic’ is also poorly defined,” they said, “partly because the critical levels at which hypoxic responses are observed depend upon the taxa involved, and to a certain extent the environment. We recommend that 'hypoxic' and 'hypoxia' should be used only with respect to living (i.e. not fossil) organisms, and that only the other '-oxic' terms should be applied to describe the oxygen status of environments.”

Removing “hypoxic” from their environmental lexicon, Tyson and Pearson proposed to keep “anoxic” for a zero level of oxygen and to use new terms, ranging from low to high concentrations: “suboxic” (0 to 0.2 ml/l), “dysoxic” (0.2 to 2 ml/l) and “oxic” (2 to 8 ml/l). Note that the units, milliliters per liter (ml/l) are used in place of the more common milligrams per liter (mg/l). For practical purposes, 1.0 ml/l equals 1.4 mg/l.

Although Tyson and Pearson’s proposal generated debate and their paper is still cited today, their recommendations for new terminology did not gain widespread acceptance.

In 2008, two Spanish researchers, Raquel Vaquer-Sunyer and Carlos Duarte, took aim at the 2 mg/l threshold for hypoxia. They examined 872 published experiments involving 206 species reporting either oxygen thresholds or lethal limits. They found a huge variation in oxygen effects. At the high end, the median lethal oxygen concentration (LC50) was 8.6 mg/l for the sensitive larvae of Atlantic rock crab. At the other end of the scale, adult Eastern oysters survived anoxic (0 mg/l) conditions for a considerable period of time.

A commonly used threshold

The vast majority of studies, some 99 percent, used 2 mg/l as the experimental threshold when measuring how long organisms could survive at a low-oxygen level — even though most species in the studies showed lethal or sublethal effects at much higher concentrations, they said.

“Whereas the conventional 2 mg/liter (threshold) may signal levels of hypoxia at which fisheries collapse, the results presented here show that it is inadequate as a threshold to conserve coastal biodiversity, because significant mortality would have already been experienced by many species,” they concluded.

“In particular, most fish and crustaceans would be lost before the oxygen content of the waters reaches the threshold of 2 mg/liter for these waters to be considered hypoxic by conventional criteria,” they said. “Currently used thresholds of hypoxia are not conservative enough to avoid widespread mortality losses and need to be critically revised.”

The two researchers proposed a “precautionary limit” of 4.6 mg/l, which would maintain populations for all but the most sensitive crab species and “effectively conserve marine biodiversity.” Other thresholds, they added, could be applied to species at risk in specific waterways, taking into account potential differences between laboratory findings and natural conditions.

Two years later, in 2010, a team of six leading experts issued an exhaustive discussion of low-oxygen dynamics with a summary of low-oxygen conditions throughout the world. They defended the use of the word “hypoxia” when talking about waterborne species while rejecting a uniform definition in terms of concentration.

“Aquatic ecologists have borrowed the term ‘hypoxia’ (low oxygen) from the medical community, but the meaning and processes are the same,” they said in the journal Biogeosciences. “The medical condition is where the body is deprived of adequate oxygen. Similarly, a water body can be deprived of adequate oxygen…

“There is no single defined concentration at which marine, coastal or estuarine waters become hypoxic to the resident organisms, nor is there consistency in units of oxygen used to express hypoxia.”

The effects of hypoxia — including behavioral, physiological and reproductive — depend on the species, stage of life and history of exposure to low oxygen, the researchers said. Therefore, multiple definitions and differing units of measure are acceptable in the scientific world.

“Most aquatic ecologists and oceanographers would agree that there is no ‘conventional’ definition of hypoxia and that the relevant thresholds are context-dependent,” they contended, adding that hypoxia can be defined for any given study, provided that the information is clearly presented.

Recent studies

A new study, published last month (March) in the journal Nature Climate Change, focuses on low-oxygen damage to coral reefs around the world, and the 22 authors seem to support the argument for abandoning 2 mg/l as any sort of overall threshold for hypoxia, particularly for coral reefs.

Lethal thresholds for tropical reef organisms can be as high as 4 mg/l, and sublethal thresholds can be even higher, especially in conditions of warmer water, according to the report, which looked at 32 experimental sites on 12 coral reefs around the globe.

For their study, the researchers defined four hypoxia thresholds beginning with “weak hypoxia” at less than or equal to 5 mg/l, which they said would include 90 percent of the sublethal effects observed among bottom-dwelling organisms in temperate waters. The other levels were “mild hypoxia” at or below 4 mg/l, “moderate hypoxia” at or below 3 mg/l, and “severe hypoxia” for the conventional 2 mg/l and below.

“Nearly all reefs in our study (84%) experienced weak hypoxia, while 50%, 34% and 13% experienced mild, moderate and severe hypoxia, respectively, at some point during the data collection period,” they said.

“Notably, oxygen loss and hypoxic events are not occurring in isolation from other stressors,” they said. “Oxygen and temperature are tightly linked in terms of organism metabolism and together may severely limit species performance.”

Higher temperatures trigger increased respiration among reef species, causing declines in oxygen and increased acidification, all leading to heightened stress and greater risks of mortality for a multitude of species. Climate change is expected to increase the frequency, duration and intensity of hypoxia in all four categories, as more “mild” events cross the threshold into “moderate,” and “moderate” events become “severe hypoxia,” according to their findings.

The definition of hypoxia may undergo further refinements in the future, but the worldwide challenge remains the same: to improve the marine environment and reduce the effects of low oxygen, hypo-oxia, or hypoxia.

This article was funded in part by King County in conjunction with a series of online workshops exploring Puget Sound water quality.

Up next: Our series continues with a look at the causes of low oxygen in Puget Sound.

View the entire series.