Annual hypoxia does not appear to be a natural condition for marine waters except for those systems previously
described. Even in Chesapeake Bay, which had hypoxia
when oxygen measurements were first made in the
1910s in the Potomac River (Sale and Skinner, 1917)
and 1930s in the main stem channel (Officer et al.,
1984), the geological record suggests that low oxygen
was not an annual, seasonally persistent feature of the
system prior to European colonization (Cooper and Brush,
1991; Zimmerman and Canuel, 2000). Geochronologies
from the hypoxic area on the continental shelf of the northern Gulf of Mexico also indicate that the current seasonal
hypoxia, which can cover over 20,000 km
2
, did not form
annually prior to the 1950s (Sen Gupta et al., 1996), and
models indicate not earlier than the 1970s (Justić et al.,
2001, Scavia et al., 2003; Turner et al., 2006). Hypoxia
was recorded with the first oxygen measurement made in
the area in the summer of 1973 on the central Louisiana
continental shelf (Rabalais et al., 2002) and remains an
annual event.
Many systems that are currently hypoxic were not so
when first studied. For systems with historical data from
the first half of the twentieth century, declines in oxygen
concentrations started in the 1950s and 1960s for the
northern Adriatic Sea (Justić et al., 1987), between the
1940s and 1960s for the northwest continental shelf of
the Black Sea, and in the 1970s for the Kattegat (Baden
et al., 1990). Declining dissolved oxygen levels were
noted in the Baltic Sea as early as the 1930s (Fonselius,
1969), but it was in the 1950s that hypoxia became
widespread (Karlson et al., 2002). Other systems had
hypoxia since the beginning of oxygen measurements,
for example, in the 1900s for Kamak Bay, Korea
(Lim et al., 2006); 1910s for Oslofjord, Norway
(Mirza and Gray, 1981); 1920s for Thames Estuary,
England (Andrews and Rickard, 1980); 1930s for Chesapeake Bay (Newcombe and Horne, 1938); and 1970s for
the northern Gulf of Mexico (Turner et al., 2008).
The negative effects of hypoxia include loss of suitable
and required habitat for many bottom-dwelling fishes and
benthic fauna, habitat compression for pelagic fishes,
direct mortality, increased predation, decreased food
resources, altered trophic energy transfer, altered bioenergetics (physiological, development, growth, and reproductive abnormalities), and altered migration. These
result in stressed fisheries species (Jørgensen, 1980;
Caddy, 1993; Rabalais and Turner, 2001; Cheng et al.,
2002; Kodama et al., 2002; Breitburg et al., 2009).
Increasing nutrient loads that also change the nutrient
ratios can affect the composition of the phytoplankton
community and can shift trophic interactions (Turner
et al., 1998). Hypoxia also alters or interrupts ecosystem
functions and services such as nutrient cycling and bioturbation (Gutiérrez et al., 2000; Rabalais, 2004; Nizzoli
et al., 2007; Middelburg and Levin, 2009; Weissberger
et al., 2009; Sturdivant et al., 2012). Much of the alteration
in functions from hypoxia can be observed in time-lapse
videos captured with Wormcam by Sturdivant
et al. (2012).
The frequency and duration of hypoxic events vary
among systems, over time, and with varying nutrient loads
or organic accumulation. Hypoxia ranges from aperiodic
events with years to decades between reoccurrences to
a persistent year-round feature that can last for years or
centuries at a time. Dominant faunal responses differ by
type of hypoxia (Figure 4). Aperiodic hypoxia, resulting
from unusual or uncommon climate conditions, elicits
the most dramatic response of mass mortality in sessile
and, at times, mobile species. For benthic invertebrates,
this dramatic response is due to the large numbers of sensitive species usually present prior to the hypoxic event.
For example, the onetime hypoxic event in the New York
Bight in 1976 that covered about 1,000 km
2 caused mass
mortality of many commercial and noncommercial
species (Boesch and Rabalais, 1991).
Summary
Hypoxia occurs in a wide range of systems and varies in
temporal frequency, seasonality, and persistence. In temperate latitudes, bottom waters can remain hypoxic or
anoxic for hours to months during summer and autumn.
There is no doubt that the increase in the areas within
coastal and open oceans with hypoxia is real. Coastal
water quality with regard to oxygen is currently on the
decline, and the future, based on the continued increase
in the global occurrence of hypoxia and current and
projected increased loads of nutrients, is trending to more
hypoxia. The formation of hypoxic areas has been exacerbated by any combination of interactions that increase primary production and accumulation of organic carbon
leading to increased respiratory demand for oxygen below
a seasonal or permanent pycnocline.
The overall forecast is for hypoxia to worsen, with
increased occurrence, frequency, intensity, and duration.
The consequences of global warming and climate change
are effectively uncontrollable at least in the near term. On
the other hand, the consequences of eutrophicationinduced hypoxia can be reversed if long-term, broadscale, and persistent efforts to reduce substantial nutrient
loads are developed and implemented. The need for water
and resource managers to reduce nutrient loads even if at
a minimum, to maintain the current status, is critical in
view of globally expanding hypoxia.
Anoxia, Hypoxia, And Dead Zones, Figure 3 Global distribution of documented cases of hypoxia related to human activities, red
dots. Systems that have recovered from hypoxia through management of nutrient and organic loadings are blue dots. Systems
that are eutrophic and in danger of becoming hypoxic are yellow dots. The number of hypoxic areas is cumulative for the successive
time periods (From Diaz et al., 2010).
ANOXIA, HYPOXIA, AND DEAD ZONES
25
described. Even in Chesapeake Bay, which had hypoxia
when oxygen measurements were first made in the
1910s in the Potomac River (Sale and Skinner, 1917)
and 1930s in the main stem channel (Officer et al.,
1984), the geological record suggests that low oxygen
was not an annual, seasonally persistent feature of the
system prior to European colonization (Cooper and Brush,
1991; Zimmerman and Canuel, 2000). Geochronologies
from the hypoxic area on the continental shelf of the northern Gulf of Mexico also indicate that the current seasonal
hypoxia, which can cover over 20,000 km
2
, did not form
annually prior to the 1950s (Sen Gupta et al., 1996), and
models indicate not earlier than the 1970s (Justić et al.,
2001, Scavia et al., 2003; Turner et al., 2006). Hypoxia
was recorded with the first oxygen measurement made in
the area in the summer of 1973 on the central Louisiana
continental shelf (Rabalais et al., 2002) and remains an
annual event.
Many systems that are currently hypoxic were not so
when first studied. For systems with historical data from
the first half of the twentieth century, declines in oxygen
concentrations started in the 1950s and 1960s for the
northern Adriatic Sea (Justić et al., 1987), between the
1940s and 1960s for the northwest continental shelf of
the Black Sea, and in the 1970s for the Kattegat (Baden
et al., 1990). Declining dissolved oxygen levels were
noted in the Baltic Sea as early as the 1930s (Fonselius,
1969), but it was in the 1950s that hypoxia became
widespread (Karlson et al., 2002). Other systems had
hypoxia since the beginning of oxygen measurements,
for example, in the 1900s for Kamak Bay, Korea
(Lim et al., 2006); 1910s for Oslofjord, Norway
(Mirza and Gray, 1981); 1920s for Thames Estuary,
England (Andrews and Rickard, 1980); 1930s for Chesapeake Bay (Newcombe and Horne, 1938); and 1970s for
the northern Gulf of Mexico (Turner et al., 2008).
The negative effects of hypoxia include loss of suitable
and required habitat for many bottom-dwelling fishes and
benthic fauna, habitat compression for pelagic fishes,
direct mortality, increased predation, decreased food
resources, altered trophic energy transfer, altered bioenergetics (physiological, development, growth, and reproductive abnormalities), and altered migration. These
result in stressed fisheries species (Jørgensen, 1980;
Caddy, 1993; Rabalais and Turner, 2001; Cheng et al.,
2002; Kodama et al., 2002; Breitburg et al., 2009).
Increasing nutrient loads that also change the nutrient
ratios can affect the composition of the phytoplankton
community and can shift trophic interactions (Turner
et al., 1998). Hypoxia also alters or interrupts ecosystem
functions and services such as nutrient cycling and bioturbation (Gutiérrez et al., 2000; Rabalais, 2004; Nizzoli
et al., 2007; Middelburg and Levin, 2009; Weissberger
et al., 2009; Sturdivant et al., 2012). Much of the alteration
in functions from hypoxia can be observed in time-lapse
videos captured with Wormcam by Sturdivant
et al. (2012).
The frequency and duration of hypoxic events vary
among systems, over time, and with varying nutrient loads
or organic accumulation. Hypoxia ranges from aperiodic
events with years to decades between reoccurrences to
a persistent year-round feature that can last for years or
centuries at a time. Dominant faunal responses differ by
type of hypoxia (Figure 4). Aperiodic hypoxia, resulting
from unusual or uncommon climate conditions, elicits
the most dramatic response of mass mortality in sessile
and, at times, mobile species. For benthic invertebrates,
this dramatic response is due to the large numbers of sensitive species usually present prior to the hypoxic event.
For example, the onetime hypoxic event in the New York
Bight in 1976 that covered about 1,000 km
2 caused mass
mortality of many commercial and noncommercial
species (Boesch and Rabalais, 1991).
Summary
Hypoxia occurs in a wide range of systems and varies in
temporal frequency, seasonality, and persistence. In temperate latitudes, bottom waters can remain hypoxic or
anoxic for hours to months during summer and autumn.
There is no doubt that the increase in the areas within
coastal and open oceans with hypoxia is real. Coastal
water quality with regard to oxygen is currently on the
decline, and the future, based on the continued increase
in the global occurrence of hypoxia and current and
projected increased loads of nutrients, is trending to more
hypoxia. The formation of hypoxic areas has been exacerbated by any combination of interactions that increase primary production and accumulation of organic carbon
leading to increased respiratory demand for oxygen below
a seasonal or permanent pycnocline.
The overall forecast is for hypoxia to worsen, with
increased occurrence, frequency, intensity, and duration.
The consequences of global warming and climate change
are effectively uncontrollable at least in the near term. On
the other hand, the consequences of eutrophicationinduced hypoxia can be reversed if long-term, broadscale, and persistent efforts to reduce substantial nutrient
loads are developed and implemented. The need for water
and resource managers to reduce nutrient loads even if at
a minimum, to maintain the current status, is critical in
view of globally expanding hypoxia.
Anoxia, Hypoxia, And Dead Zones, Figure 3 Global distribution of documented cases of hypoxia related to human activities, red
dots. Systems that have recovered from hypoxia through management of nutrient and organic loadings are blue dots. Systems
that are eutrophic and in danger of becoming hypoxic are yellow dots. The number of hypoxic areas is cumulative for the successive
time periods (From Diaz et al., 2010).
ANOXIA, HYPOXIA, AND DEAD ZONES
25