The ecological consequences of marine hypoxia: from behavioural to ecosystem responses

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Stressors in the Marine Environment. Edited by Martin Solan and Nia M. Whiteley
© Oxford University Press 2016. Published in 2016 by Oxford University Press.
2011). Our appreciation of how ecosystems are chang-
ing is complicated by the ‘shifting baseline syndrome’—
the problem of recognizing natural, relatively unspoilt
reference habitats against which all current and future
ecosystem states can be measured— addressed by Shep-
pard (1995). Meanwhile, however, due to our vast foot-
print, both spatially and temporally, experts question
the existence and/or use of natural reference points
today. A particular example is the long history and tre-
mendous impact of modern industrial sheries (since
about 1880) on marine ecosystems (e.g. Callum, 2007);
this also mirrors new knowledge in the eld of historical
ecology that humans signicantly altered many coastal
marine environments centuries and even millennia ago
(Rick and Erlandson, 2008). Oxygen deciencies have
become a major global stress factor to estuarine and ma-
rine environments, based on their potential to act as a
primary driver of ecosystem collapse and on the rapid-
ity of their effect. The present contribution summarizes
key ndings to provide an overview of the far-reaching
consequences of anthropogenically induced deoxygen-
ation in our seas, with special focus on coastal systems.
10.2 Coastal hypoxia and anoxia: turning
‘normal’ into ‘extreme’ habitats
‘When you can’t breathe, nothing else matters.’
This old motto by the American Lung Association ex-
presses best the seriousness of oxygen depletion as an
environmental issue (Diaz, 2001). Oxygen is funda-
mental for sustaining aerobic life, and despite the dis-
coveries of numerous subsystems that bypass aerobic
pathways, this life physically and biologically struc-
tures most marine habitats. Thus, the worldwide in-
crease in hypoxic (low dissolved oxygen DO; in coastal
bottom waters traditionally ≤ 2 ml l-1, but see Section
10.2.2 for discussion on different hypoxia thresholds)
10.1 Welcome to the Anthropocene!
The Greek philosopher Heraclitus of Ephesus is re-
ported to have said ‘nothing endures but change’, and,
indeed, the biological world is changing rapidly. The
rapidity and magnitude of these changes are mirrored
in a suggested new, currently informal, designation
for this period in Earth history - the Anthropocene
(Crutzen and Stoemer, 2000). This is because the pace
and sheer spectrum of drivers behind changes in the
biosphere can be traced to a single hub, humankind.
Our ngerprint is everywhere, or to use a new catch-
word, our footprint is enormous and has tended to
atten everything in its path, both guratively and lit-
erally. Our inuence has gone beyond the habitats we
actually inhabit to encompass the entire globe and even
beyond (man-made space debris orbiting our planet).
Humans have altered marine environments and af-
fected marine organisms from the shoreline to the deep
sea. When looking at Halpern etal.’s (2008) global map
of human impacts, it is difcult to nd any part of the
world’s oceans that has not been affected. It is not only
our activities in the marine environment that affect life
in the sea—it’s also our actions and behaviour on land.
Combined effects of habitat destruction, overshing,
introduced and invasive species, warming, acidica-
tion, pollution, and massive run-off of anthropogenic
nutrients are transforming complex ecosystems, clear
and productive coastal seas, and complex food webs
into monotonous seabeds, dead zones (areas with insuf-
cient oxygen to sustain most metazoan life, Diaz and
Rosenberg, 2008), and into simplied, microbially domi-
nated ecosystems (Jackson, 2008).
Instead of describing how ecosystems work, marine
ecologists are increasingly describing why things now
work differently: nearly half of all the scientic publica-
tions in a range of subelds are devoted to describing
the deterioration and suggesting solutions (Rose etal.,
CHAPTER10
The ecological consequences
ofmarine hypoxia: from behavioural
toecosystem responses
Bettina Riedel, Robert Diaz, Rutger Rosenberg, and Michael Stachowitsch

176 STRESSORS IN THE MARINE ENVIRONMENT
In contrast, the ‘off-on’ or ‘all-or-nothing’ property of
typical, recurring oxygen depletion with a compara-
tively shorter duration (i.e. days to months) makes
affected areas more unstable than ‘extreme’ habitats:
little adaptation is possible and a minimalistic set of
opportunistic and tolerant species tend to dominate.
10.2.1 Hypoxia: occurrence, development,
andcrux of the matter
Life on Earth emerged under anaerobic conditions,
and low-oxygen environments are ancient phenom-
ena: the modern oxic world apparently represents an
exceptional state of the atmosphere–ocean system on
our planet (Strauss, 2006). Nonetheless, the most re-
cent geological eon, the Phanerozoic (542 mya to the
present; rise of the metazoan world), is also marked
by a long series of widespread oxygen deciencies in
the global ocean or parts of it. These were often associ-
ated with mass extinction events, for example the Late
Permian mass extinction (Wignall and Twitchett, 1996),
series of short-lived abiotic recoveries related to shifts
back to ocean anoxia in the Triassic (Grasby et al.,
2012), or multiple black shale depositions during the
Cretaceous. The duration of such oxygen deciency
episodes ranged from a few thousand to millions of
years (see references in Gooday etal., 2009, on both
geological and more recent historical records).
and anoxic (0 ml DO l-1) areas in coastal marine ecosys-
tems over the past decades (Diaz and Rosenberg, 2008)
is an alarming signal. It underlines the loss of marine
biodiversity and complex and profound changes in
ecosystem properties/functions (e.g. productivity, de-
composition rates, nutrient cycling, and resistance or
resilience to perturbations) and services (e.g. climate
regulation, recreation, and food supply) (see Sala and
Knowlton, 2006; Worm etal., 2006; Palumbi etal., 2008
and references therein). The signs are clear in nearshore
waters and, alarmingly, now also in the open ocean
(mid-water oxygen minimum zones, OMZs; Stramma
etal., 2010; see Section10.2.1). Ongoing eutrophication
and/or climate change is predicted to further exacer-
bate the situation in the future (Rabalais etal., 2009).
Although some areas are already experiencing the
worst-case scenario many other of the world’s coastal
ecosystems may increasingly be approaching tipping
points (Fig.10.1). The result will be a new set of ex-
treme habitats (Stachowitsch etal., 2012). Traditional
‘extreme’ habitats such as deep-sea hydrothermal
vents or hot springs are typically characterized by a
single inhibitive parameter at the far end of the natu-
ral range (e.g. temperature, salinity, pH, or hydrogen
sulphide). Such parameters, however, are typically re-
main stable here over long periods of time, i.e. decades
to millennia enabling adaptation by the often complex
communities inhabiting them (e.g. Wharton, 2002).
Figure10.1 The interactive and cumulative effects of multiple stressors increasingly force marine coastal systems to a critical tipping point and
qualitatively altered state.
biodiversity, ecosystem function, and services
intact
ecosystem
pollution overexploitation eutrophicationhabitat destruction
species invasionsdisease harmful algal blooms
climate change
marine debris
dead zone
tipping point

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 177
surface waters from mixing to the bottom. The duration
of the stagnation is decisive: when oxygen consump-
tion rates of bottom organisms exceed those of resup-
ply, hypoxia and subsequent anoxia develop. Examples
of coastal areas susceptible to the formation of oxygen
depletion include shallow and semi-enclosed seas, estu-
aries, deep fjords, and silled basins (e.g. fjords in the Sk-
agerrak area, northern Europe, Rosenberg, 1980; central
parts of the Baltic Sea, Zillén etal., 2008).
In contrast to what occurs in OMZs, much of the
coastal oxygen depletion has developed in the last 50
years and is closely associated with anthropogenic ac-
tivities. Coastal hypoxia was a rather localized prob-
lem until the 1950s, generally associated with sewage
discharges or industrial outows in areas with a semi-
enclosed hydrogeomorphology. Since the 1960s, how-
ever, reported cases of hypoxic sites have doubled
in each decade (Fig. 10.2) and, increasingly, shallow
continental seas were affected (e.g. Gulf of Mexico
and Kattegat) (Diaz, 2001; Diaz and Rosenberg, 2008).
Increasing population growth, intensied develop-
ment, and expansion of agricultural activities (e.g.
increasing use of industrially produced fertilizers),
especially in the temperate zone, led to a twofold in-
crease in the global ux of nitrogen (N; Galloway etal.,
2004) and a two- to threefold greater phosphorus ux
(P; Howarth etal., 1995) to coastal waters. This excess
nutrient input to aquatic ecosystems (eutrophication)
stimulates primary production and enhances the ow
of organic water to the seaoor, fuelling microbial res-
piration and amplifying oxygen depletion (Rabalais
etal., 2002). Importantly, shallow water communities
are, as opposed to those in OMZs, less adapted to low
DO and have, except for a few, highly resistant species,
much higher oxygen tolerance thresholds (see Sec-
tion10.2.2). Anthropogenic eutrophication has multi-
pronged impacts. On the one hand it fuels positive
feedback loops such as hypoxia-induced enhanced
ammonium (NH4+) and phosphate uxes to the overly-
ing water, which in turn sustain high rates of primary
production (changes in biogeochemical processes
upon hypoxia are summarized in Kemp etal., 2009, or
Middelburg and Levin, 2009). On the other hand, the
cycle of decomposition of dead organic material fuels
microbial respiration, which causes further mortalities.
Thus, eutrophication of coastal seas has the potential
to exacerbate conditions in areas already predisposed
to oxygen depletion or to tip previously unaffected
systems into hypoxia (e.g. Conley etal., 2009).
Several studies have demonstrated a correlation
over time between anthropogenic eutrophication and
the occurrence of hypoxia/anoxia in coastal areas. The
Low oxygen waters also occur naturally in the
world’s oceans today. Oxygen minimum zones (OMZs;
DO concentration < 0.5 ml l-1), on the one hand, are
widespread and stable (periods greater than decadal
scales) low-oxygen features at intermediate depths
(typically 100–1200 m) in the open ocean, intercepting
the continental margins primarily along the eastern Pa-
cic, off southwest Africa, in the Arabian Sea and in
the Bay of Bengal (Levin, 2003; Rabalais etal., 2010).
OMZs cover about 30 million km2 of open ocean, but
their depth and thickness of occurrence, i.e. the upper
and lower depth boundaries, are variable and depend
on natural processes and cycles, e.g. circulation and
oxygen content of the respective ocean region (Helly
and Levin, 2004). The principal formation drivers are
high surface and photic (light) zone productivity, a
limited circulation, and old water masses (Levin etal.,
2009; Rabalais etal., 2010): the bacterial degradation of
decaying organic matter that sinks from the productive
shallow oceans to the deep increases the oxygen con-
sumption and thus decreases oxygen concentration in
the water column, while the poor water exchange re-
stricts oxygen supply from surface waters. Often OMZs
are associated with western boundary upwelling re-
gions where oxygen-depleted but nutrient-rich water
fuels primary production—the primary contributor to
persistent hypoxia under upwelling regions. Where ox-
ygen minima impinge on the seaoor, organisms have
adapted their behaviour, morphology, and/or their
metabolism/enzymatic processes over geological time
to either permanently or temporarily (diel vertical mi-
gration) survive at (for more information see Childress
and Seibel, 1998; Levin, 2003; Levin etal., 2009). The
temporary encounter with hypoxic waters from OMZs
or upwelling systems in coastal areas (e.g. off the coast
of Chile, west Africa, or India), however, causes simi-
lar effects as human-induced coastal hypoxia (see Sec-
tion10.3) with severe impacts on local organisms (e.g.
Levin etal., 2009 and references therein).
Most coastal oxygen depletions (critical DO concen-
tration ≤ 2 ml l-1 versus < 0.5 ml l-1 in OMZs), on the
other hand, are smaller, variable in size, seasonal (for
other duration classes and coastal hypoxic threshold
concentrations see Section 10.2.2) and typically as-
sociated with a particular bottom topography and/
or hydrogeomorphology. Combined with a density or
thermal stratication of the water column because of
freshwater discharge from rivers (pycnocline: transition
layer that separates less saline surface water from more
saline/denser bottom water) or heating of the ocean sur-
face layer during calm and warm periods (thermocline),
this restricts water exchange and prevents oxygen-rich

178 STRESSORS IN THE MARINE ENVIRONMENT
(total area > 245 000 km2, i.e. larger than the United
Kingdom) had been identied as being eutrophication-
related hypoxic (Diaz and Rosenberg, 2008; Fig.10.2).
The latest global assessment has brought the total to
over 600 coastal areas affected (Diaz etal., 2013). Hot-
spots of oxygen deciencies include Chesapeake Bay
and the Gulf of Mexico, USA, Scandinavian and Baltic
waters, and the Black Sea, as well as Chinese/Korean/
Japanese waters (e.g. UNEP, 2006; STAP, 2011; Diaz
etal., 2013).
Single areas have reached enormous dimensions.
The Baltic Sea and the Gulf of Mexico, for example,
harbour the two largest anthropogenic hypoxic zones
worldwide, covering a mean area of 49 000 and 17 000
km2 (maximum 67 000 km2/22 000 km2), respectively
(Turner etal., 2008; Savchuk, 2010). At the other end
of the range are small-scale hypoxias in unexpected
locations. In McMurdo Sound (Southern Antarctic),
for example, the untreated sewage from the US Ant-
arctic research centre led to organic enrichment in the
1990s with subsequent benthos reduction (Conlan
etal., 2004); recently, hypoxia most likely triggered by
climate change was reported from the Eastern Antarc-
tic (Powell etal., 2012). These polar examples point to
shallow (< 50 m), semi-enclosed Northern Adriatic,
Mediterranean Sea, provides a good example for this
connection. Oxygen depletions, often associated with
massive marine snow events (decaying organic mate-
rial that sinks from higher in the water column), have
been noted here periodically for centuries (Danovaro
etal., 2009 and references therein), but their frequency
and severity have markedly increased in the second
half of the twentieth century due to high anthropogenic
input of nutrients via the Po River, Italy. In the North-
ern Adriatic, echoing the global phosphorus ux noted
above, the inputs of N and P increased by ve and three
times, respectively, between 1945 and 1985. This was re-
ected in an average long-term decrease in water body
transparency (by 4–6 m), an increase in surface-water
oxygen concentrations produced by phytoplankton
blooms, and decreasing bottom oxygen concentrations
(Justić etal., 1987; Justić, 1988). The result has been se-
vere bottom oxygen deciencies, with impacted areas
ranging from several km2 (Stachowitsch, 1992) to ap-
proximately 4000 km2 (Stefanon and Boldrin, 1982).
Early this century, dead zones appeared on top of the
list of emerging environmental challenges (UNEP,2004),
and, in 2008, more than 400 marine systems worldwide
Figure10.2 Cumulative increase of hypoxia in coastal areas over time reported in the scientific literature
Adapted from Diaz and Rosenberg(2008).
12 +7 +6 +2 +15
+24
+71
+143
+167
+96
Cumulative number of sites
600
500
400
300
200
100
0
< 1910 1920 1930 1940 1950 1960 1970 1980 19902000–09
period of explosive increase
of coastal eutrophication
(doubling of hypoxic sites)

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 179
use of a wide range of terms (e.g. oxic, dysoxic, sub-
oxic, anoxic; aerobic, dysaerobic, quasi-aerobic, anaer-
obic; hypoxic, normoxic), depending on whether these
expressions are applied to environments, biofacies, or
the physiological responses of living organisms, and
whether additional stress factors are involved, such
as the development of sulphidic (euxinic) conditions
(Tyson and Pearson, 1991).
Aquatic ecologists traditionally determine the
onset of hypoxic conditions as the point when most
organisms become physiologically stressed and/or
show sublethal avoidance reactions (see Section10.3).
Breitburg et al. (2009), for example, dene hypoxia
mechanistically as ‘oxygen concentrations that are
sufciently reduced that they affect the growth, re-
production, or survival of exposed animals, or result
in avoidance behaviors’. The traditional critical oxy-
gen concentration dening hypoxia in shallow coastal
seas and estuaries is thereby often set at at ≤ 2 ml l−1,
equivalent to 2.8 mg DO l−1 or 91.4 µM (see for exam-
ple Diaz and Rosenberg, 1995; Wu, 2002). Others de-
termine hypoxia at DO ≤ 2 mg l−1 (1.4 ml DO l−1 or 63
µM; e.g. Rabalais etal., 2001; Gray etal., 2002; Vaquer-
Sunyer and Duarte, 2008). For the most recent com-
pilation of thresholds, ranges, and technical terms,
see Table1 in Altenbach etal. (2012). The sensitivity
of organisms, however, varies with physical factors
such as temperature or salinity, and with biological/
taxon-specic factors such as life habits, mobility, life
cycle stage, or physiological adaptations to hypoxia or
tolerance to hydrogen sulphide (H2S) (e.g. Hagerman,
1998; Vaquer-Sunyer and Duarte, 2010, 2011). Moreo-
ver, the duration, intensity, extent, and frequency of
hypoxia/anoxia can also modulate the critical oxygen
range limits of organisms.
According to the temporal scale, hypoxia types are
classied into (from Diaz and Rosenberg, 1995, 2008):
• Seasonal: yearly events lasting from weeks to
months, typically associated with summer or au-
tumnal water column stratication (e.g. Chesapeake
Bay Mainstem, USA, Ofcer et al., 1984; Gulf of
Mexico shelf, USA, Rabalais etal., 2007)
• Periodic: hours to days, i.e. diel cycles in shallow
estuaries and tidal creeks caused by 24-h cycles
of water column photosynthesis and respiration,
or lunar neap–spring tidal cycles modulating the
stratication intensity (e.g. York River estuary, USA,
Nestlerode and Diaz, 1998; Delaware coastal bays,
USA, Tyler etal., 2009)
• Episodic:infrequenteventsatintervals>1year,pre-
vailing for weeks, often the rst indication that an
a close match between the distribution of dead zones
and the widening global human footprint. It is now in
east and south Asia where the United Nations Environ-
ment Programme (UNEP) expects the steepest increase
in the number of coastal hypoxic sites in the upcoming
years due to population growth and increases in the
magnitude and changes in nutrient ratios in river ex-
port (STAP,2011).
Climate change can make marine systems more sus-
ceptible to the development of hypoxia due to direct
effects on the water column stratication, precipita-
tion patterns, and temperature. Gilbert et al. (2010),
for example, determined a faster decline in oxygen
rates over the last three decades within a 30 km band
near the coast than in the open ocean (> 100 km from
shoreline) between 0 and 300 m water depth. How-
ever, there is also evidence that oxygen concentrations
in the global open ocean are declining as well (Helm
et al., 2011). Stramma et al. (2010), for example, re-
ported horizontally and vertically expanding OMZs
in the tropical Pacic, Atlantic, and Indian Oceans
during the past few decades. This has been attributed
most likely to lower oxygen solubility due to surface-
layer warming and the weakening of ocean overturn-
ing and convection (Keeling et al., 2010). Recently,
oxygen decrease and shoaling of the oxic–hypoxic
boundary has been observed on the southern Califor-
nian shelf (Bograd etal., 2008). Off the Oregon coast,
previously unreported hypoxia has been documented
on the inner shelf since 2000 (Chan etal., 2008). Impor-
tantly, other stressors such as rising temperatures and
ocean acidication will team up and create synergistic
effects with deoxygenation, exacerbate the frequency,
duration, and intensity of both naturally and eutrophi-
cation-related hypoxia (Gruber, 2011), and amplify the
stress on resident organisms in both the coastal and
open ocean (e.g. Harley et al., 2006; Stramma et al.,
2010; Bopp etal., 2013; for examples see Section10.4).
Thus, understanding hypoxia and its effects on eco-
systems requires several perspectives, starting at the
local level, moving to regional scale, and nally to a
global perspective (Diaz etal., 2013).
10.2.2 Definitions and thresholds: we can agree
to disagree
The terminology and units used to dene hypoxia and
anoxia, as well as the conventional denition of when a
critical oxygen concentration is reached, vary between
and within earth and life sciences and their subdisci-
plines (Rabalais etal., 2010). This has led to the selected

180 STRESSORS IN THE MARINE ENVIRONMENT
recruitment, species diversity, biological interactions,
trophic dynamics, and community structure to sedi-
ment geochemistry and habitat complexity (e.g. sum-
marized in Diaz and Rosenberg, 1995; Wu, 2002; Gray
etal., 2002; Middelburg and Levin, 2009; Levin etal.,
2009) (Fig.10.3). Every component of the marine en-
vironment is affected—fauna and ora, pelagos and
benthos, from bacteria to macrofauna organisms. Hy-
poxia therefore threatens biodiversity and alters eco-
system structure and function (Solan etal., 2004; Worm
etal., 2006). The response to oxygen depletion can go
beyond replacing a given community with another
one (i.e. species replaced by others with similar eco-
logical roles). In the worst-case scenario, mass mortali-
ties change formerly vital and rich coastal ecosystems
into taxonomically and functionally depauperated,
microbial ones (Sala and Knowlton, 2006). Finally,
apart from the ecological consequences, hypoxia also
negatively inuences the social and economic activi-
ties related to ecosystem services provided by marine
ecosystems, e.g. tourism and sheries (e.g. STAP,2011;
Diaz etal., 2013).
Here we present the ecological consequences of
hypoxia/anoxia at the various levels. Importantly,
these biological responses act in concert and therefore
always require a holistic approach in both understand-
ing and responding to this phenomenon.
10.3.1 Individual- and population-level effects
Environmental change or stress, even if it inuences the
performance and tness of organisms, is not inherently
ecosystem is severely stressed (e.g. Gullmarsfjord,
Sweden, Nilsson and Rosenberg, 2000), or
• Permanent:yearstodecadestocenturies(e.g.parts
of the Baltic Sea, Conley etal., 2011).
A meta-analysis by Vaquer-Sunyer and Duarte (2008)
shows the enormous variability in oxygen thresholds
for lethal responses to oxygen depletion among benthic
organisms: median lethal concentration (LC50) thresh-
olds ranged from 8.6 mg DO l−1 for the rst larval zoea
stage of the crustacean Cancer irroratus, to persistent re-
sistance to anoxia for the oyster Crassostrea virginica at
a temperature of 20 °C. Accordingly, no ‘conventional’
threshold is universally applicable or can fully cover
the range of biological/environmental stages or situ-
ations. In fact, ‘biological stress’ occurs well above the
traditional oxygen limits noted above, with effects of
hypoxia on growth and behaviour observed at oxygen
concentrations near 6.0 mg l−1 and impacts on other
metabolic components near 4 mg DO l−1 (Gray etal.,
2002). Vaquer-Sunyer and Duarte (2008) determined,
in 90% of the 872 experiments analysed, a median le-
thal oxygen concentration at < 4.59 mg DO l−1.
10.3 Impact of hypoxia in coastal
environments: the ecological implications
Responses at the molecular level, leading to physi-
ological and metabolic adaptions, are the initial or-
ganismic responses to low oxygen concentrations.
Then, cascading effects, direct and indirect, can trig-
ger changes at levels ranging from behaviour, growth,
ecosystem
community
population
species
molecule
multi-level responses
abundance & biomass
physiology/metabolism & behaviour
feeding & growth
predation & competition
changes in: reproduction & recruitment
shifting community structures (homogenization & depauperation)
decrease in biodiversity & local/regional extinction
loss of ecosystem function & services
severity,
duration,
frequency
of hypoxia
Figure10.3 Cascading effects of oxygen depletion, triggering individual responses which in turn affect population attributes, community
dynamics, and ultimately biodiversity and ecosystem integrity.

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 181
areal extent affected. Accordingly, the distances may
range from centimetres to metres to kilometres. Meio-
fauna, for example, typically responds with a decrease
in burial depth (e.g. Alve and Bernhard, 1995) and
sometimes even oats up into the water column until
normoxic conditions are re-established (Wetzel etal.,
2001). Macroinfauna typically emerges onto the sedi-
ment surface. Well-known examples of this behaviour
include sea urchins (i.e. Echinocardium cordatum: Nils-
son and Rosenberg, 1994; Schizaster canaliferus: Riedel
etal., 2014), polychaetes (Pihl etal., 1992), bivalves (i.e.
Solecurtus strigilatus, Laevicardium sp., Ensis ensis: Hrs-
Brenko etal., 1994), and burrowing crustaceans (i.e. the
mantis shrimp Squilla mantis: Stachowitsch, 1992). The
latter were even observed swimming in the water col-
umn (Stachowitsch, 1984). Note that the mantis shrimp
and other commercially important burrowing crusta-
ceans such as Nephrops norvegicus normally emerge
onto the sediment surface only during the night (and
are then shed), but under hypoxic conditions are also
present on the sediment during the daytime (Baden
etal.,1990).
For less mobile epifauna, unable to escape or avoid
hypoxic waters, hypoxia typically induces a range
of species-specic behavioural changes that involve
changing the body shape or position. This includes
raising the respiratory structures higher in the water
column to avoid low oxygen concentrations near
the sediment surface (i.e. arm-tipping brittle stars,
bad. It is part of life and in fact a motor of evolution. Dis-
turbances in environmental conditions at certain levels
and frequencies (e.g. intermediate disturbance hypothe-
sis; Connell, 1978) can set positive impulses, but in most
other cases the outcome for the resident species and
communities will be negative (e.g. Pearson and Rosen-
berg, 1978; Harley etal., 2006; Halpern etal., 2008).
In terms of hypoxia, marine organisms have evolved
two general and non-exclusive coping mechanisms.
Firstly, they can respond with physiological adaptions.
These can include lowered metabolism, effective use of
respiratory pigments, increased ventilation rate and/
or blood ow, and switch to anaerobic metabolism
(Hagerman, 1998). These strategies are treated sepa-
rately in Chapter2 of this volume. Secondly, and gener-
ally the rst visible sign of defence, animals can change
their behaviour to either increase oxygen supply or
decrease oxygen demand. The sensitivity, mobility, and
tolerance of marine organisms determine their expo-
sure and reaction to intermittent or chronic hypoxia.
Depending on the animal’s lifestyle, such behaviour
primarily involves avoidance strategies: ‘run for your
lives’ (migration of more mobile fauna to a normoxic
refuge). If this is not possible, it’s ‘only the strong sur-
vive’ (with specic behavioural responses of sessile and
less mobile fauna to reduce hypoxic stress, Fig.10.4).
Migration to more oxygenated areas can occur both
vertically and horizontally. The former mirrors the
oxygen gradient in the water column, the latter the
arm-tipping body elongation emergence
aggregation
discarding “ballast”
max. surface area : volume ratio
Figure10.4 Typical avoidance responses of sessile and less mobile benthic macrofauna to hypoxia. Upper left to lower right: arm-tipping brittle
star, body elongation in sea anemones, emergence from sediment by infaunal sea urchins, aggregation of cryptic species (e.g. small crabs) on
elevated substrate, increase in surface area:volume ratio in holothurians, epifaunal sea urchins discard protecting/camouflaging material (i.e. shells
and debris), and hermit crabs leave their protective shells.

182 STRESSORS IN THE MARINE ENVIRONMENT
from chronic and episodic (upwelling events) hypoxia
in the Neuse River Estuary, North Carolina, USA (Bell
and Eggleston, 2005). In the Gulf of Mexico, in the ab-
sence of physical barriers to movement, evading or-
ganisms (i.e. brown shrimp Farfantepenaeus aztecus and
several nshes) aggregated just beyond (1–3 km) the
margins of the hypoxic zone (2.0 mg l−1 contour; Craig,
2012). This example points to another, indirect lethal ef-
fect of hypoxia, namely the enhanced susceptibility of
brown shrimp and non-target nshes to the commer-
cial shrimp trawl shery. This effect is probably most
intense within a relatively narrow region along the
hypoxic edge (Craig, 2012), mirroring a more general
observation that shers often detect hypoxia/anoxia
events based on unusual catches of species normally
not caught together (Stefanon and Boldrin, 1982). Else-
where, sh come to the surface and into shallowest
waters. In Mobile Bay, Alabama, in the Gulf of Mexico,
for example, such hypoxia-induced aggregation events
have historically been termed ‘jubilees’ because local
residents could collect the still-living sh in knee-deep
water along the beach (Loesch, 1960).
Importantly, while avoidance reactions may help
organisms to escape or survive hypoxia longer, they
rarely promote individual performance or population
structure. Unusual and unexpected migrations (or al-
tered, typically extended, migration paths), for exam-
ple, can quickly reduce an organism’s energy reserves,
especially if accompanied by reduced food acquisition.
Potentially altered abiotic factors (i.e. temperature or
salinity) or food availability in the new refuge area
may further lower body condition and tness. In the
Columbia River Estuary on the Oregon–Washing-
ton border, USA, the Dungeness crab Cancer magister
avoided, i.e. migrated away from, water with < 50%
oxygen saturation and reduced its food intake in such
hypoxic waters; this effect, coupled with reduced sa-
linity (the animals are weak osmoregulators), caused
the crabs to reduce feeding, ingestion, and pumping
water over their gills, impairing performance and
growth (Roegner etal., 2011).
Any change or shift in the spatial distribution of
benthic organisms—whether it be migration to a new
region, shallower burial depth, or exposure atop an
elevated substrate—may adversely affect survival
and render stressed fauna more vulnerable to preda-
tors (and human exploitation). Apart from shers,
who may change their shing patterns to take advan-
tage of faunal aggregations at the margins of hypoxic
zones (e.g. Tolo Harbour, Hong Kong; Fleddum et
al., 2011), natural predators with a higher tolerance
to low DO conditions than prey organisms (and/or
siphon-stretching bivalves, or tiptoeing crustaceans;
e.g. review by Diaz and Rosenberg, 1995), or maxi-
mizing the surface area:volume ratio to minimize the
diffusion distances within tissues and improve oxy-
gen diffusion (i.e. sea anemones: Shick, 1991). Organ-
isms may try to reach any elevated substrate above the
sediment surface (i.e. bioherm-associated crabs such
as Pilumnus spinifer or Pisidia longicornis emerge from
hiding and aggregate on top of sponges and ascidians;
Stachowitsch, 1984; Haselmair etal., 2010). This is be-
cause the oxygen gradients on the seaoor are often
very steep, and moving only a few centimetres can
mean the difference between tolerable and lethal condi-
tions. Other behaviours may serve to increase mobility
and/or reduce oxygen demand by discarding ‘addi-
tional ballast’ when exposed to environmental stress.
The decorator crab Ethusa mascarone and the sea urchin
Psammechinus microtuberculatus, for example, discarded
their protecting camouage when confronted with low
DO concentrations (Haselmair etal., 2010; Riedel etal.,
2014). Similarly, hermit crabs emerge from their shells
and move about fully exposed (Stachowitsch, 1984;
Pretterebner etal., 2012).
Numerous laboratory and eld observations world-
wide underline the similarity of such key behavioural
responses to hypoxia. Thus, the responses of represent-
atives with certain life habits in one system provide a
window into comparable interpretations of benthic
health/status elsewhere. This would be one further
new and intriguing aspect to the much-discussed
early concept of ‘parallel level-bottom communities’
(Thorson, 1958). Arm-tipping in ophiuroids is a case
in point. The same posture has been observed for Am-
phiura chiajei, A. liformis, and Ophiura albida in the Kat-
tegat (Rosenberg et al., 1991; Vistisen and Vismann,
1997), Ophiura texturata in the North Sea (Dethlefsen
and von Westernhagen, 1983), Ophiothrix quinquemacu-
lata in the Northern Adriatic (Stachowitsch, 1984; Rie-
del etal., 2014), and brittle stars in the Gulf of Mexico
(Rabalais etal., 2001).
The more mobile taxa (mostly sh and crustaceans)
can escape to surface waters overlying the bottom hy-
poxic layer or to the margins of the hypoxic zone. In
Tolo Harbour, Hong Kong, for example, hypoxia occurs
seasonally (strong stratication during the wet season,
monsoon) and most benthic epifauna escapes to more
oxygenated open waters in summer and returns again
in winter (Fleddum etal., 2011). Sometimes a migration
is so extensive that it leads to a (not mortality-related)
defaunation of a population in the hypoxic site, as re-
ported for the blue crab Callinectes sapidus and oun-
ders Paralichthys dentatus and P. lethostigma escaping

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 183
a population. In Bornholm Basin, Southern Baltic, for
example, only adult individuals of the bivalve Astarte
borealis were found after a decade-long stagnation and
largely hypoxic conditions (Leppäkoski, 1969); in Kiel
Bay a similar age-class shift was observed for Astarte
elliptica, Mya arenaria, and Cyprina islandica (Rosenberg,
1980).
Tolerance to hypoxia may be also based upon al-
lometric issues, with smaller individuals in and
between species reported to be more tolerant of
hypoxia (e.g. in yellow perch Perca avescens, Robb
and Abrahams, 2003). Nonetheless, the organism
size (or weight) effect on hypoxia tolerance is mixed.
Shimps etal. (2005), for example, investigated how
vulnerability to hypoxia changes across sh size in
spot (Leiostomus xanthurus) and Atlantic menhaden
(Brevoortia tyrannus). While for the Atlantic menha-
den, smaller sh were consistently more tolerant to
hypoxia than larger sh, the converse effect was ob-
served for spots (i.e. larger individuals were more
vulnerable than their smaller conspecics). The
authors attribute this to a mix of mechanisms and
therefore call for an approach integrating lethal and
sublethal effects, direct and indirect effects, and sh
behaviour. Other studies reported no correlation be-
tween hypoxia tolerance and size (e.g. Wagner etal.,
2001). Thus, size can affect hypoxia tolerance, but
the effect may be species-specic. Note also that the
presence of smaller individual sizes, both of single
species and of entire communities, can also reect
early stages of growth during the recovery process
after mass mortalities.
10.3.2 Community-level effects
Changes at the community level emerge from pro-
cesses operating at the individual level. Here, the
impact of hypoxia and anoxia on a particular species
triggers cascading series of direct and indirect effects
on the overall biota, which by denition are linked in
one way or the other (O’Gorman etal., 2011). Thus,
beyond reducing growth, disrupting life cycles, alter-
ing behaviour, and changing biological interactions,
hypoxia may signicantly reduce abundance, bio-
mass, and diversity in marine ecosystems. As noted
above, there is a high intra- and interspecic vari-
ability in tolerance to hypoxia, with some individu-
als/taxa already experiencing mortality at an oxygen
concentration where others do not even show visible
signs of stress (Vaquer-Sunyer and Duarte, 2008; Rie-
del etal., 2012; see Section 10.3.1). In a generalised
pattern of community response, mild (approximate
that can swim faster) can also exploit the moribund
fauna in hypoxic areas (Pihl et al., 1992). Sometimes,
unusual behaviours that do not involve migration or
full exposure to predators can also increase predation
pressure. Well-known examples include abnormal
extension of siphons or of the palps of bivalves and
polychaetes above the sediment surface, which are
then bitten off by foraging predators (e.g. Sandberg
et al., 1996). It sometimes pays to look upwards as
well: vertical escape to near-surface waters can also
increase the predation risk from diving birds (see ref-
erences in Domenici etal., 2007). However, it is not
always the predator that can benet from hypoxia.
Oxygen deciencies may also create predation ref-
uges for more tolerant prey species, e.g. enhanced
prey survivorship of more hypoxia-tolerant quahog
clam Mercenaria mercenaria, softshell clam Mya are-
naria, and blue mussel Mytilus edulis from less tol-
erant predators such as crabs, the sea star Asterias
forbesi, or the oyster drill Urosalpinx cinerea (Altieri,
2008). An intermediate scenario also exists when both
predator and prey are affected. Here, relative toler-
ance will govern predation efciency (Breitburg etal.,
1994). In the Northern Adriatic, for example, more
tolerant anemones were able to utilize a ‘window of
opportunity’ during sinking oxygen concentrations
to feed on moribund brittle stars (Riedel etal., 2008,
2014). A weakened intraspecic interaction strength
can also increase predation-induced mortality. For
example, altered sh school structure (e.g. increas-
ing school volume, i.e. space between individual sh)
and dynamics (e.g. changing the shufing behav-
iour within the school) may affect school integrity in
terms of synchronization and execution of antipreda-
tor manoeuvres (Domenici etal., 2002). Thus, differ-
ent tolerance levels and changes in both predator and
prey behaviour at low DO may modify their relation-
ships and potentially alter the population structure of
communities.
Hypoxic effects can also manifest themselves as re-
duced feeding and growth (sh: Brandt et al., 2009;
diatom Skeletonema costatum: Wu etal., 2012) and can
lower reproductive capacity (crustacean: Brown-Peter-
son etal., 2008). In most aquatic species, early life his-
tory stages are the most sensitive in a life cycle—one
reason why the use of early life stages (of sh, for ex-
ample) has been suggested in establishing water-qual-
ity criteria or screening chemicals. Reduced survival
in larvae and juveniles under hypoxia (e.g. the oyster
Crassostrea virginica: Widdows etal., 1989; Baker and
Mann, 1992) can shift the overall population age in fa-
vour of adult life stages, affecting the sustainability of

184 STRESSORS IN THE MARINE ENVIRONMENT
of hypoxia markedly limits macrobenthic produc-
tion and thus transfer to higher trophic levels. The
decrease in macrobenthic production may be par-
ticularly detrimental during critical periods when
epibenthic and demersal predators have high-energy
demands. A more detailed picture of how oxygen de-
pletion can alter the relative importance of different
trophic pathways within a community is provided
by Munari and Mistri (2011). The authors studied the
effect of short-term hypoxia (24 h, < 2 mg DO l-1) on
predation by the muricid gastropod Rapana venosa
(hypoxia-tolerant) on three bivalve species: Scapharca
inaequivalvis (adapted to hypoxic conditions with an-
aerobic metabolism), Tapes philippinarum (responding
with a decrease in burial depth and siphon exten-
sion), and Cerastoderma glaucum (hypoxia-sensitive).
Under normoxia, the gastropod had a marked pref-
erence for S. inaequivalvis. Under hypoxia, however,
the predator switched to the more easy-to-catch T.
philippinarum. Thus, hypoxia facilitates the coexist-
ence of two more-hypoxia-tolerant bivalves because
the predator switches prey. The hypoxia-sensitive C.
glaucum is ‘the net loser of the game’: it is predated—
if not preferentially—under normoxia, and becomes
moribund/dies at hypoxia.
To minimize competition with superior individu-
als or to avoid being targeted by predators, (prey)
species generally use avoidance strategies or main-
tain a safe distance. With ongoing duration of oxy-
gen depletion, however, these intra- and interspecic
interaction strengths can weaken. The unusual,
dense aggregation of organisms on top of elevated
substrates as a hypoxia-avoidance mechanism is
a good example. The crab Pilumnus spinifer, for ex-
ample, is territorial and preferentially preys upon
small adult crabs and brittle stars in the Adriatic.
Target organisms usually avoid the sponges and
ascidians inhabited by the crab or ee. The almost
uniform avoidance response to hypoxia, i.e. climbing
on higher substrates to reach more oxygenated areas,
however, diminishes this safe distance within and
between species. It apparently outweighs normal
agonistic behaviour and predator–prey relationships
(Haselmair etal.,2010).
Many natural communities are characterized by,
and depend on, a single or a functional group of
habitat-forming foundation species (ecosystem en-
gineers) that provide the framework for the entire
community (Crain and Bertness, 2006). Stachowitsch
(1984) provides an example of how the loss of one
such species can trigger a cascade of secondary mor-
talities with major impacts on community functioning
DO concentration > 1 ml l-1) and short-term hy-
poxia may therefore primarily involve quantitative
losses—in the sense of punctuated, species-specic
mortalities— rather than fundamentally altered over-
all community structure and composition. Longer-
lasting or more intense hypoxia, however, threatens
to depauperize and functionally homogenize benthic
communities (Sala and Knowlton, 2006); in a worst-
case scenario, the macrofauna is eliminated entirely
(Stachowitsch, 1984).
Going from species to next higher taxonomic levels,
distinct patterns of sensitivity/tolerance emerge. The
literature reveals, as a broad generalization, that sh
are the most sensitive group, followed by crustaceans,
polychaetes, echinoderms, sea anemones, molluscs,
hydro-/scyphozoans, and ascidians (Vaquer-Sunyer
and Duarte, 2008; Riedel etal., 2012). The broad con-
sensus is that:
• larvalstagesaremorevulnerabletolowoxygencon-
centrations than their corresponding adults (Gray
etal., 2002);
• macrofaunaismoresensitivethanmeiofauna(Josef-
son and Widbom, 1988);
• epifauna is more vulnerable than infauna because
tolerance to low oxygen and sulphide in marine
species is closely correlated to the in situ levels they
are generally exposed to (Vistisen and Vismann,
1997);and
• mobile forms are more vulnerable than sessile
forms, in line with their apparently decreased toler-
ance for both physiological and physical stress (Sa-
gasti etal.,2001).
The effects on the individual and species level—
ranging from benthic invertebrates to shes—change
the complex interactions between species and can
derail community dynamics. Even if the benthic
community does not suffer extensive mortality, func-
tionally important biological interactions such as
trophic dynamics may be fundamentally altered (see
above). Sturdivant etal. (2014), for example, assessed
the effects of seasonal hypoxia on macrobenthic pro-
duction in Chesapeake Bay and its three main trib-
utaries from 1996 to 2004. The results showed 90%
lower macrobenthic production during hypoxia (≤ 2
mg DO l-1) relative to normoxia. The biomass loss of
ca. 7000–13 000 metric tons of organic carbon over an
area of 7700 km2 was estimated to equate to a 20−35%
displacement of the Bay’s macrobenthic productiv-
ity during the summer. While the higher consum-
ers may benet from easy access to stressed prey
in some areas, the large spatial and temporal extent

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 185
hotspots’ form a discrete community from the sur-
rounding soft sediment habitat and provide substrate
for larval settlement and epigrowth, shelter, and food.
The mortality of key component species, such as a
large sponge, accelerates mortality of the associated
fauna in a positive feedback loop during hypoxia/
anoxia (Fig.10.5). Such rapid mortality stands in con-
trast to the recovery, which can be delayed for decades
even after signicant increases in bottom water oxygen
concentrations (e.g. Northern Adriatic: Stachowitsch,
and stability: in the northeastern Adriatic, the benthic
macroepifauna largely consists of interspecic ag-
gregations termed multi-species clumps (Fedra etal.,
1976). Their presence and distribution depends on the
initial presence of shelly material for the settlement
of larval invertebrates. Here, the settled sessile lter-
and suspension feeders (mostly sponges, ascidians,
or bivalves) serve as an elevated substrate for addi-
tional mobile and hemi-sessile organisms, i.e. brittle
stars, holothurians, and decapods. These ‘biodiversity
a
c
b
d
e
g
f
h
Figure10.5 a–h Behavioural responses and mortality of benthic macrofauna after oxygen depletion in the Northern Adriatic Sea,
Mediterranean: (a) emerged and dead organisms on beach including from lower left to upper right flatfish, burrowing shrimp, gobiid, and bivalve;
(b) emerged bivalves (
Corbula gibba
) on the sediment, in the centre dead crab (carapace) and large bivalve; (c) nocturnal mantis shrimp
Squilla
mantis
emerges during day and also swims into water column—note dark colour of the sediment; (d) emerged, moribund sipunculid and dead
and decomposing gobiid fish; (e) emerged bivalve with cast-off siphon; (f) dead female swimming crab with eggs—multi-generational impact of
hypoxia; (g) ‘Black spot’ indicates remains of former multi-species clump—note empty sea urchin test; (h) post-anoxia condition—bivalve and sea
urchin test as potential substrate for future epigrowth. Photos: M. Stachowitsch, except for f (department photo archive, author unknown). Time-
lapse films showing the effects of oxygen depletion on benthic macrofauna during and after experimentally induced hypoxia available at: http://
phaidra.univie.ac.at/o:87923 and http://phaidra.univie.ac.at/o:262380 [PLATE 9]

186 STRESSORS IN THE MARINE ENVIRONMENT
may depend more on the presence of key functional
types than on species richness itself (Thrush et al.,
2006). This calls for examining the potential effect of
hypoxia on key functional groups, e.g. the ecosystem
engineers mentioned above.
Ecosystem engineers alter their physical surround-
ings or change the ow of resources through their
presence or activity (e.g. feeding or burrowing),
thereby creating or modifying habitats and inuenc-
ing all associated species. They therefore signicantly
contribute to and inuence ecosystem biodiversity,
functions, and stability. The role of such ecosystem
engineers may persist on time scales longer than their
individual lifetimes. On structurally less complex soft-
bottom surfaces, for example, dominant sessile organ-
isms can create new habitat enabling the establishment
of entire epifaunal communities that would otherwise
be unable to persist. Examples include the above-men-
tioned bivalve/oyster beds, coral reefs, the Northern
Adriatic sponge-, bivalve-, and ascidian-dominated
multi-species clumps, or tube-building polychaetes.
Among the infauna, abundant bioturbators—such
as the irregular sea urchin Schizaster canaliferus in the
Northern Adriatic—may determine the 3D complexity
in the sediment (Schinner etal., 1997).
Benthic suspension feeders play a key role in the en-
ergy transfer, nutrient (re)cycling, and sedimentation
or resuspension of particulate organic matter (POM)
in coastal ecosystems. In shallow systems with mod-
erate water exchange, the feedback processes between
the benthic and the pelagic subsystems are more im-
mediate. Such a quicker and more direct interaction,
specically that involving nutrient exchanges, has
been termed benthic–pelagic coupling (reviewed by
Graf, 1992). When the benthic and pelagic subsystems
closely adjoin, the macrobenthos—consisting largely
of lter- and suspension-feeders such as sponges,
bivalves, ascidians, tube worms, and brittle stars—
directly controls the pelagic biomass and production
through grazing. Depending on water depth, they can
lter the entire volume of a basin within days to weeks
(e.g. 3 d, Laholm Bay, Sweden, Loo and Rosenberg,
1989; 20 d, Gulf of Trieste, Northern Adriatic, Ott and
Fedra, 1977). In the context of hypoxia/anoxia, such
benthic communities play a regulatory role that has
been termed a ‘natural eutrophication control’ (Of-
cer etal., 1982). In removing most of the suspended
material in the overlying water column, they convert
pelagic biomass into benthic biomass with a lower
respiration/biomass ratio, thus stabilizing the entire
system and controlling water quality (Hily, 1991).
Moreover, biodeposits (i.e. faeces, pseudofaeces, and
1991; case studies from the Adriatic Sea, the Black Sea,
Danish estuaries, and Delaware Bay, USA, summa-
rized in Steckbauer etal., 2011). Community develop-
ment is further impaired by harmful shing activities,
which remove or destroy this benthic 3D complexity,
and by renewed oxygen depletions. The net result is
marked longer-term community degradation (i.e. bio-
diversity loss) and decreased habitat complexity. Such
interactions between habitat/community degradation
and hypoxia have also been observed in other biogenic
habitats. Oyster beds, for example, create physically
complex habitats, important to estuarine biodiversity
and shery production. Deeper parts of the beds can
experience hypoxia events, whereby mass mortality of
the bivalves impacts the abundance, distribution, and
diversity of associated sh and invertebrates (Leni-
han and Peterson, 1998). Hypoxia-induced habitat
degradation can in turn impact remote, undisturbed
surrounding habitats (i.e. through the movement and
abnormal concentration of refugee organisms that
have subsequent strong trophic impacts, Lenihan
etal., 2001), triggering a domino effect of widespread
ecosystem degradation.
Finally, lower-diversity communities (including re-
duced competition for resources and habitat in defau-
nated areas) provide a niche for more rapidly growing,
opportunistic colonizers (e.g. Pearson and Rosenberg,
1978). They are also less resistant to invasive species; in
the Chesapeake Bay, for example, the cover by the tu-
nicates Botryllus schlosseri and Molgula manhattensis, the
polychaete Ficopomatus enigmaticus, and the anemone
Diadumene lineata—all four now found worldwide—
was highest on settling plates exposed to moderately
low oxygen (DO 2-4 mg l-1) (Jewett etal., 2005).
10.3.3 Ecosystem-level effects
The increasing intensity of human disturbance in pro-
ductive coastal marine ecosystems is triggering un-
precedented habitat and biodiversity loss. This raises
concerns about whether ecosystem function and eco-
system services provided to humanity can be main-
tained under such severe disturbance (UNEP,2006).
The complexity of marine ecosystem structure and
dynamics is based on the interactions of the component
species, the food web connections across trophic levels,
and the landscape modications induced by biotic–
abiotic interactions. Hypoxia affects all three levels.
Intuitively, high diversity maintains high complexity of
interactions and feedbacks among species, promoting
stability and resistance to invasion or other forms of
disturbance. Often, however, ecosystem performance

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 187
sedimented POM) are a source of food for bacteria
and meio- and macrofauna organisms, promoting sec-
ondary production in the benthos and increasing the
nutrient turnover (Graf, 1992). Most suspension feed-
ers are relatively long-lived, with a low mobility, and
characterized by spatial variability but temporal sta-
bility. The loss of such stabilizing compartments due
to oxygen crises unbalances ecosystem dynamics and
makes the whole system more vulnerable to additional
perturbations.
Hypoxia and the corresponding loss of biodiversity
also signicantly affect bioturbation, another major
process conducted by benthic ecosystem-engineering
macrofauna (Sturdivant etal., 2012). Bioturbation in-
cludes all transport processes and their physical ef-
fects on the substrate, along with particle reworking
and burrow ventilation (reviewed by Kristensen etal.,
2012). Bioturbators affect the sediment permeability
and water content, break up chemical gradients in pore
water, and subduct organic matter. This, in turn, inu-
ences organismic biomass, remineralization rates, and
the inorganic nutrient efux—all vital for primary pro-
duction. The burrowing and ventilation activities lead
to a complex mosaic of reduced and oxidized zones
in the sediment, substantially affecting biogeochemi-
cal properties and processes (for a description of the
complex interactions of biogeochemical cycles that ac-
company eutrophication and hypoxia, see Middelburg
and Levin, 2009).
Key functional processes translate into positive and
negative effects cascading from bacteria/microalgae,
to meiofauna, and macrofauna/-algae, potentially ex-
tending in the food chain to sh and birds (Kristensen
etal., 2012). Eutrophication-induced die-offs of benthic
suspension feeders and bioturbators disrupt impor-
tant benthic–pelagic uxes and signicantly impair
ecosystem function and services (Solan etal., 2004). Ul-
timately, broad-scale losses may trigger a vicious cycle
via accumulation of organic material on the sea oor,
increased microbial decomposition, decreased bottom
water DO, nutrient release from the sediment to water
column, accelerated primary production, and—back
to step one—increased ow of organic material to the
sea oor.
Diversity loss (i.e. reduced number of genes, spe-
cies, or functional groups) due to oxygen depletion is
determined by multiple factors ranging from sensitiv-
ity to low DO to the presence of additional stressors.
The multiple layers of interactions and feedbacks, hid-
den drivers, and emergent properties, however, make
the consequences of species loss for ecosystem func-
tion difcult to predict. High-diversity communities,
comprising a wide range of functional traits, can ef-
ciently capture biologically relevant resources (e.g. nu-
trients, light, or prey), produce biomass, decompose,
and recycle essential nutrients. The loss of biodiversity
may initially only minimally impact ecosystem func-
tion: when some individuals of one species die, then
individuals of another species but same functional trait
can ll the gap (quantitative loss but compensatory re-
sponse). Ultimately, however, the rates of change will
accelerate. When dynamics are shaped by engineering
species, a few strong interactions dominate (Ellison
etal., 2005). Here, the loss of even a single key species
can immediately and profoundly affect other species
and ecosystem processes, whereby the order in which
species are lost is also important (Solan etal., 2004).
Systems with little functional redundancy are therefore
relatively fragile and susceptible to even small pertur-
bations: the loss of key engineers is likely to lead to
rapid, possibly irreversible shifts in biodiversity and to
system-wide changes in structure and function (Eben-
man and Jonsson, 2005). Importantly, substituting one
species with another from the same functional guild
does not imply uninterrupted, full efciency: ecosys-
tem structure and functional processes may weaken or
change long before the engineering compartment itself
disappears completely. The suspension-feeding capac-
ity is a case in point. A particular species typically l-
ters a certain range of particle sizes. When a species is
lost, that particle size range may no longer be ltered
out, which—from the view of the overall lter-feeding
capacity—represents a qualitative change in function
(i.e. altered spectrum of particle sizes ltered out by
remaining species) (Riedel etal., 2012).
Hypoxia can therefore alter community composi-
tion, inuence overall ecosystem properties and ul-
timately trigger a regime shift (an often irreversible
shift between two alternate stable environmental
states) (e.g. Conley etal., 2009). Suspension feeders
might be replaced by deposit feeders, macrobenthos
by meiobenthos, and bioturbators may be lost, caus-
ing functional homogenization at the community
level (Thrush etal., 2006). In a study on eight million
years of uctuating hypoxia during the Late Juras-
sic, for example, Caswell and Frid (2013) report that
less intense hypoxia was associated with signicant
changes in species composition but not in biological
traits, implying the retention of ecological function.
In periods of extremely different oxygen conditions,
however, traits suggestive of opportunists (e.g. more
surface-living and shallow-burrowing species, and
thinner skeletons) and altered function occurred.
More generally, under hypoxic stress Wu (2002)

188 STRESSORS IN THE MARINE ENVIRONMENT
however, even micromolar (µMol) concentrations of
hydrogen sulphide are highly toxic; they inhibit cyto-
chrome c oxidase and impair pulmonary function and
oxygen transport, negatively affecting the aerobic en-
ergy supply (Nicholls and Kim, 1982). During oxygen
depletion events, the reduced layer of the sediment
migrates towards the sediment surface and sulphate
reduction is fuelled by the abundant dead organic
material on the sea oor. This can result in a relatively
rapid build-up of H2S in the sediment and the over-
lying water column, reducing the survival times in
marine benthic communities by an average of 30%
(meta-analysis by Vaquer-Sunyer and Duarte, 2010,
involving 30 macrofauna species from 10 groups). The
authors also reported a higher effect of sulphide on the
survival of eggs than for juvenile or adult stages. More
examples of the combined effects of hypoxia, hydrogen
sulphide, and/or ammonia (also acutely toxic to ma-
rine organisms) are reviewed by Gray etal. (2002).
Equally, exposure to higher temperatures may also
make marine benthic organisms more vulnerable to
hypoxia because of the lower oxygen solubility (with
increasing temperature and salinity) but increasing
metabolic rates and thus oxygen requirement (Brown
etal., 2004). Juvenile Atlantic sturgeon (Acipenser oxy-
rinchus), for example, displayed a more severe mor-
tality response to hypoxia (< 4 mg DO l-1) at 26 °C
(mortality 92%) compared to 19 °C (22%) (Secor and
Gunderson, 1998). A correlation between hypoxia
tolerance and temperature was also found in spot
(Leiostomus xanthurus), Atlantic menhaden (Brevoortia
tyrannus) (Shimps etal., 2005), and Atlantic cod Gadus
morhua (Schurmann and Steffensen, 1992); in juvenile
summer ounder Paralichthys dentatus, the combina-
tion of low DO levels (50-70% air saturation) and high
temperature (30 °C) severely reduced growth rates (Sti-
erhoff etal., 2006). A meta-analysis assessing the effects
of an expected maximum temperature increase of 4 °C
during the twenty-rst century on hypoxia thresholds
for coastal benthic macrofauna (Vaquer-Sunyer and
Duarte, 2011) highlights this threat: the prediction is a
decrease in survival time under hypoxia by 74% and
an increase in the threshold oxygen concentrations for
mortality by 25.5%. Although these predictions repre-
sent worst-case scenarios, they generate concerns for
the future of coastal communities in a globally chang-
ing world where considerable warming of both air and
sea is projected (IPCC, 2007).
Organisms exposed to hypoxia are commonly con-
fronted simultaneously with acidication (hyper-
capnia) stress: respiration reduces oxygen, leads to
elevated carbon dioxide (CO2) levels in the water, and
suggests a general shift from K-selected (i.e. large
body size, long life expectancy, with few offspring)
to r-selected, often opportunistic species (i.e. high
fecundity, small body size, early maturity onset, and
fast generation times), and from complex to simple
food chains. Such scenarios represent undisputable
worst-case situations for biodiversity and ecosystem
function. The result is local extinction (Solan etal.,
2004) and large-scale (functional) homogenization
at increasingly lower levels (‘microbialization’; Sala
and Knowlton, 2006).
10.4 Interplay and synergy of multiple
stressors
Despite the gravity of hypoxia and anoxia as stres-
sors of marine systems, they remain only one of the
many listed at the onset of this contribution. Most
marine ecosystems are clearly affected by the inter-
active and cumulative effects—additive, synergistic,
and antagonistic—of multiple human stressors (Crain
et al., 2008). The multi-level effects (i.e. physiology,
morphology, ecology, individual- to ecosystem-level,
etc.) of even a single stressor on marine ecosystems are
often difcult enough to understand. Determining the
cumulative effects of multiple stressors, however, is a
major challenge (but note, for example, interactions be-
tween effects of oxygen depletion and chemicals such
as heavy metals or pesticides reviewed in Holmstrup
etal., 2010). We restrict ourselves here to stressors that
are increasingly being studied in combination with the
effects of exposure to oxygen deciency such as hydro-
gen sulphide (H2S), higher temperatures, and/or a
lowered pH.
Sulphate, for example, is always present in the ma-
rine anoxic sediment layers, and certain bacteria (e.g.
Beggiatoa spp. or Desulfovibrio spp.) typically use or-
ganic compounds such as lactate, pyruvate, and short-
chain fatty acids as energy and carbon sources to reduce
sulphate to sulphide (Jørgensen and Fenchel, 1974). In
general, the level and distribution of H2S largely de-
pends on the sediment type (i.e. muddy sediment is
easily stratied and is anoxic a few millimetres below
the surface, compared to well-oxygenated coarser sedi-
ments) and on the amount of organic material present.
Infaunal species therefore typically encounter not only
transient low dissolved oxygen conditions but also
elevated H2S levels. Some organisms have evolved
physiological and metabolic adaptions to survive days
or even weeks in sulphidic habitats (reviewed in Gries-
haber and Völkel, 1998). For most aerobic organisms,

THE ECOLOGICAL CONSEQUENCES OF MARINE HYPOXIA 189
Acknowledgements
We are grateful to anonymous reviewers for insight-
ful comments that helped improve the quality of the
chapter.
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