Chapter 10
Oxygen Movement in Seagrasses
Jens Borum*, Kaj Sand-Jensen, Thomas Binzer and Ole Pedersen
Freshwater Biological Laboratory, University of Copenhagen, Helsingørsgade 51,
DK-3400 Hillerød, Denmark
Tina Maria Greve
National Environmental Research Institute, Ministry of Environment and Energy,
Vejlsøvej 25, DK-8600 Silkeborg, Denmark
I. General Introduction
Seagrasses are, like all vascular plants, obligate aer-
obes, which require a continuous supply of oxygen
to sustain aerobic metabolism of both above- and
below-ground tissues. Compared to their leaves, sea-
grass roots and rhizomes may experience oxygen de-
privation for shorter periods, but these below-ground
tissues exhibit physiological adaptations which al-
low them to rely temporarily on anaerobic fermenta-
tive metabolism (Pregnall et al., 1984; Smith et al.,
1988). Aerobic respiration is energetically about 10
times more efficient than fermentative processes,
which tend to accumulate ethanol, acetate, and other
potentially toxic metabolites representing a threat
to tissue survival (Smith et al., 1988; Crawford and
Braendle, 1996). The meristematic tissues, located
in the transition between water column and sediment,
are especially vulnerable to low oxygen supply and
exposure to anaerobic metabolites due to their high
metabolic activity and the continuous oxygen sup-
ply required for mitotic growth. In addition to the
importance of oxygen inside seagrass tissues, main-
tenance of oxic conditions around roots may pro-
vide efficient protection against invasion of reduced
toxic compounds and metal ions from the surround-
ing sediment (Armstrong et al., 1992; Crawford and
Braendle, 1996; see also Marb´a et al., Chapter 6).
Accordingly, there are several benefits to plant per-
formance in maintaining a rich oxygen supply to all
tissues including roots and rhizomes.
∗Author for correspondence, email: jBorum@bi.ku.dk
In most terrestrial plants oxygen is readily sup-
plied from the atmosphere and from aerated soils.
However, emergent wetland plants rooted in water-
logged soils or submerged macrophytes, such as sea-
grasses, must temporarily or permanently endure
conditions with low supplies of oxygen from the
surrounding environment. Coastal marine sediments
are mostly anoxic and highly reduced because of the
degradation of organic matter within the sediment
and slow oxygen diffusion from the water column.
Hence the sediment represents a strong oxygen sink
rather than a source, and oxygen must be supplied to
below-ground tissues of seagrasses either by photo-
synthesis or by oxygen diffusing from the water col-
umn through leaves to rhizomes and roots (Pedersen
et al., 1998). The slow diffusion of oxygen in water
(10,000 times slower than in air) contributes to the
potential risk of oxygen deprivation in submerged
plants. Firstly, transport of oxygen from the water
column through the relatively thick diffusive bound-
ary layers around leaves is impaired by the slow rate
of diffusion, and secondly, liquid phase oxygen dif-
fusion inside plants is grossly inadequate to support
oxygen transport over long distances such as those
between leaves and root tips. Therefore, submerged
plants have become anatomically adapted to oxygen
shortage by developing aerenchymatic tissues with
continuous air-filled lacunae running from leaves to
roots (Armstrong, 1979; Larkum et al., 1989; Kuo
and den Hartog, Chapter 3).
This chapter aims to present the current status
of knowledge with respect to oxygen production,
consumption and transport within seagrasses. We
255–270.A. W. D. Larkum et al. (eds.), Seagrasses:Biology, Ecology and Conservation, pp.
c
2006Springer. Printed in the Netherlands.
256 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
describe and evaluate the techniques, which have
been used for estimating or directly measuring oxy-
gen variability and transport in seagrasses. Next, we
address the internal and external sources of oxygen,
sinks of oxygen and transport of oxygen between
tissues. We demonstrate the factors controlling in-
ternal oxygen variability by means of manipulations
under controlled conditions in the laboratory and
present data on in situ oxygen variability from sea-
grass stands. Finally, we briefly discuss the potential
coupling between seagrass oxygen dynamics and the
occurrence of die-off events in seagrass beds.
II. Measuring Oxygen Dynamics
and Transport
A. Difficulties in Measuring Oxygen Dynamics
and Transport
Measuring oxygen production, consumption, release
and transport in seagrasses and other rooted macro-
phytes is a major technological challenge. A number
of different techniques are available and have been
applied, but all methods seem to have potential draw-
backs depending on the specific objective. The in-
trinsic problems are related to the fact that all rates of
oxygen exchange within plants depend on a complex
of factors such as (1) the immediate size of oxygen
pools within specific plant tissues and in the media
surrounding leaves and roots, (2) the resistance to
transport within plants and between plant and me-
dia, and (3) the steepness of gradients within tissues
and between tissues and the surrounding media. The
factors vary temporally and spatially under natural
conditions and these changes are difficult to control
and mimic in the laboratory. Assessment of oxygen
dynamics within and around seagrasses under con-
trolled laboratory conditions is, therefore, best suited
for describing relative rates and mechanisms rather
than determining absolute rates as they would occur
under natural conditions.
B. Chamber Techniques
Oxygen release and consumption have traditionally
been assessed by measuring changes in bulk water
Abbreviations
DBL – diffusive boundary layer
KPa – kilo Pascals
Rubisco – Ribulose-1,5-bisphosphate carboxylase-oxygenase.
oxygen concentrations in incubation chambers. This
technique is feasible for measurements of photosyn-
thesis and respiration of isolated leaves, although
potential problems with lacunar oxygen accumula-
tion, and especially with poor simulation of natural
boundary layer conditions around leaves, may inter-
fere significantly with rate measurements. Measure-
ments of respiration in isolated roots and rhizomes
using chamber techniques can be more problematic.
It has been argued that measuring respiration of iso-
lated below-ground tissues under aerobic conditions
may overestimate the respiration that would occur in
anoxic sediments (e.g. Smith et al., 1988; Touchette
and Burkholder, 2000). However, such a procedure
may also underestimate respiration, because the la-
cunar oxygen supply from leaves to roots and rhi-
zomes is disrupted when the tissues are separated
from the leaves. Hence, respiration has to be fueled
by oxygen diffusing from the bulk water through
boundary layers and through the more or less per-
meable root and rhizome tissues, and this diffusion
may be too slow to sustain an adequate internal oxy-
gen supply and mimic natural conditions of intact
plant gas phase transport (Saglio et al., 1984).
Chamber techniques provide reliable estimates of
whole plant metabolism if intact plants with leaves,
roots and rhizomes are incubated for longer time
intervals allowing equilibration of oxygen between
lacunae and bulk water (Kemp et al., 1986). In
addition, split chambers with leaf compartments
separated from root compartments by water- and
gas-tight seals have been used to estimate oxygen
transport from leaves to roots and subsequent oxy-
gen release to the sediments (e.g. Sand-Jensen et al.,
1982; Kemp and Murray, 1986). Results based on
this technique have, however, to be interpreted with
caution. Transport from leaves to roots is driven by
gradients between sources and sinks, and the steep-
ness of these gradients depend greatly on the exper-
imental conditions (Sorrell and Armstrong, 1994).
The oxygen gradient from the root to the sediment
is especially important, because it determines the
rate of oxygen loss to the sediment and because it
can vary by an order of magnitude depending on
the oxygen consumption within the root medium
(Sorrell and Armstrong, 1994). To mimic natural
sediments as proper sinks the rooting media must
not only be anoxic but also reducing and oxygen
consuming to generate the sufficiently steep gradi-
ents between root and sediment forcing the release
of oxygen. Such conditions can be established by
Chapter 10 Oxygen Movement in Seagrasses 257
adding titanium citrate buffer to the root medium
thereby increasing measured rates of oxygen release
from the roots (Sorrell and Armstrong, 1994). How-
ever, if simulating natural conditions properly the
split chamber techniques provide the most reliable
estimates of whole plant oxygen transport.
C. Gas Extraction Techniques
Changes in internal pools of oxygen in plants may
be more directly assessed by extracting oxygen from
the lacunar spaces of different tissues (e.g. Orem-
land and Taylor, 1976; Carlson et al., 1988). This
technique is usually destructive in the sense that tis-
sues have to be cut or squeezed to harvest internal
gases, but the method does allow assessment of diel
changes in lacunar oxygen and, in addition, extracted
air-samples can be analyzed for concentrations of
internal CO2,N
2and CH4using infrared gas analy-
sis and gas chromatography at high precision (Hart-
man and Brown, 1967; Oremland and Taylor, 1976;
Larkum et al., 1989). However, the gas extraction
technique does not allow on-line recording of in-
ternal gas dynamics as functions of changes in en-
vironmental conditions and the technique has poor
temporal and spatial resolution.
D. Microtechniques
Microelectrodes, compared to other techniques, do
provide much more elegant opportunities for on-
line assessment of internal oxygen conditions within
plants (e.g. Armstrong et al., 1994; Armstrong
et al., 2000; Greve et al., 2003). Some of the ear-
liest microelectrodes for measuring internal oxy-
gen contents in plant tissues were polarographic
electrodes requiring external reference electrodes,
and therefore oxygen could only be assessed in
the liquid phase and not in air-filled lacunae (e.g.
Bowling, 1973). The appearance of fast-responding
and stirring-independent Clark-type oxygen micro-
electrodes with built-in guard cathodes provided
the first means of microscale oxygen measurements
in both liquid and gas phase at high spatial and
temporal resolutions (Revsbech, 1989). The tech-
nique allows measurements of internal plant gradi-
ents and oxygen profiles on root surfaces at spatial
scales of 10 μm or less (Caffrey and Kemp, 1991;
Armstrong et al., 1994; Christensen et al., 1994;
Pedersen et al., 1998; Greve et al., 2003) and at
temporal scales of less than 1 s. Hence, rates of oxy-
gen release or consumption can be continuously and
precisely assessed in specific tissues under natural
or manipulated conditions. The high spatial resolu-
tion, however, has the drawback that the overview
of whole plant metabolism or oxygen release is
lost. Such processes are better determined by using
chamber techniques under proper mimicry of natural
conditions.
Microoptodes also provide means of measuring
oxygen and other compounds at high spatial and tem-
poral resolution, and, in addition, the optode tech-
nique has been developed to allow two dimensional
recording of changes in oxygen conditions in sed-
iments, microbial mats and in the rhizosphere of
aquatic plants (Glud et al., 1996). The planar op-
todes, potentially, provide excellent means for as-
sessing spatial differences in oxygen concentrations
around roots and rhizomes of intact plants as a func-
tion of experimentally altered conditions for plant
photosynthesis.
III. Oxygen Sources
The supply of oxygen to support aerobic metabolism
within seagrass tissues derives from internal oxygen
produced by photosynthesis and from passive diffu-
sion of oxygen from water column or sediment, when
oxygen partial pressures in the external media sur-
pass plant oxygen partial pressures (Fig. 1). Photo-
synthesis of seagrasses mainly takes place in the epi-
dermal cells with high chlorophyll contents assumed
to represent an adaptation to the low light conditions
often experienced by submerged macrophytes (Kuo
and McComb, 1989; Larkum et al., 1989). Rates of
photosynthesis on a dry weight basis are relatively
low for seagrasses and other hydrophytes compared
to terrestrial plants (Bowes, 1985; Nielsen and Sand-
Jensen, 1989; Larkum et al., Chapter 14). However,
high rates of oxygen evolution take place in indi-
vidual leaves which is immediately apparent as for-
mation of numerous gas bubbles during calm, sunny
days (Zieman, 1974). In addition, leaf biomass of
some seagrass beds may be very high and gross
primary production can exceed 10 g O2m−2d−1
(Ziegler and Benner, 1998; Hemminga and Duarte,
2000).
A. Oxygen Evolution by Photosynthesis
Gross photosynthesis of seagrass leaves exceeds res-
piratory demands by almost an order of magnitude
258 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
Fig. 1 . Schematic representation of the potential sources of oxygen in seagrasses. In the light, photosynthetic oxygen evolution in the
leaves is the only source of plant oxygen. In darkness, when internal leaf oxygen partial pressure declines below that of the water column,
oxygen is supplied to leaves by passive diffusion from the water. Theoretically, the sediment could be a source of oxygen, if partial
pressures in the sediment exceeded those of roots and rhizomes, but the rhizosphere of seagrasses is usually anoxic.
(Touchette and Burkholder, 2000; Larkum et al.,
Chapter 14) and generates a considerable internal
build-up of oxygen pools inside the tissues and in
leaf lacunae. Extracted gas samples from seagrass
leaves have contained oxygen of 30–35 kPa equal to
10–15 kPa above air saturation (Oremland and Tay-
lor, 1976; Roberts and Moriarty, 1987; Larkum et al.,
1989) and up to 55 kPa in other submerged macro-
phytes (Hartman and Brown, 1967). Microelectrode
techniques, similarly, have recorded high internal
oxygen partial pressures in seagrasses (Greve et al.,
2003; Borum et al., in preparation). The oxygen
partial pressure inside the meristematic region of
Zostera marina and Thalassia testudinum can in-
crease from virtually zero, reached during prolonged
darkness, to more than 40 kPa within 60–120 min at
saturating irradiances. These high internal oxygen
partial pressures in part result from the increased
proportion of oxygen in the lacunal gas and in part
by the overall increase in gas pressure inside leaf
lacunae.
High internal oxygen partial pressure may by it-
self affect seagrass photosynthesis by generating
photorespiration due to the competition between
oxygen and carbon dioxide for binding sites in
Rubisco (Søndergaard and Wetzel, 1980; Touchette
and Burkholder, 2000; Larkum et al., Chapter 14).
In the submerged macrophyte Scirpus subterminalis
photorespiration increased from about 10% of net
photosynthesis at normal external oxygen partial
pressures to 30% at external partial oxygen pressures
above 35 kPa (Søndergaard and Wetzel, 1980). The
influence of high oxygen contents on photorespira-
tion has, to our knowledge, not been examined for
seagrasses.
B. Oxygen Supply from the Surrounding Media
In the absence of photosynthetic oxygen evolution, it
has often been assumed that the aerobic metabolism
of seagrass tissues must rely on internal pools of oxy-
gen built-up during the day (Smith et al., 1984; Preg-
nall et al., 1984; Hemminga, 1998). However, oxy-
gen can readily diffuse from the water or sediment
into the plant when external oxygen concentrations
exceed internal concentrations. Oxic rhizospheres
have been reported for rosette plant communities in
oligotrophic lakes (Christensen et al., 1994; Peder-
sen et al., 1995), but usually sediments of rooted
macrophyte beds are anoxic and cannot function as
a source of oxygen for root metabolism (Armstrong,
1979). However, passive influx of oxygen from the
water column has been clearly shown to ensure in-
ternal oxygen status of seagrass tissues reflected by
sustained oxygen loss from roots to sediment during
darkness (Fig. 2; Pedersen et al., 1998), and trans-
port of oxygen from water column to root media
in the dark has also been described for submerged
Chapter 10 Oxygen Movement in Seagrasses 259
0 50 100 150
Distance to root surface (μm)
0
5
10
15
20
25
pO2, porewater (kPa)
Root surface
Steady state in light
Steady state in darkness
Fig. 2 . Steady state microprofiles of oxygen within the sediment
vs. distance to the root surface of Zostera marina measured in the
light (open symbols) and in the dark (solid symbols). Presence
of the oxygen profile in the dark, although at a lower level than
in the light, documents that oxygen is transported from the water
column, as the only possible source in the dark, through the
lacunae of leaves to rhizomes and roots, and that this source
is sufficiently strong to supply oxygen to the roots in excess of
respiratory demands (Pedersen, Borum and Greve, unpublished).
freshwater plants (Sand-Jensen et al, 1982; Sorrell
and Dromgoole, 1987).
Rates of passive influx of oxygen from water into
leaves can be calculated according to Fick’s first law
(see section III, Koch et al., Chapter 8). The influx
depends on the difference between oxygen partial
pressures outside and inside the plant (i.e. the gra-
15 20
0
250
500
750
1000
1250
15 20
Distance to leaf surface (μm)
15 20 25
Oxygen partial pressure (kPa)
0.29 cm s
-1
2.7 cm s
-1
11.2 cm s
-1
FlowFlowFlow
DBL = 440
μ
m
DBL = 210
μ
mDBL = 140
μ
m
Leaf
Fig. 3 . Oxygen profiles measured by microelectrodes on the surface of eelgrass leaves at different water flow velocities along the leaves.
The thickness of the diffusive boundary layer can be determined from the profiles showing reduced thickness with increasing flow
velocity (Peter Larsen, unpublished).
dient driving the diffusion), the traveling distance
across the diffusive boundary layer (DBL) and cu-
ticle/cell wall and the diffusion coefficients of oxy-
gen in water and tissue components (Larkum et al.,
1989; Pedersen et al., 1998). Larkum et al. (1989)
reported estimates of diffusion coefficients for cuti-
cle and cell walls and estimates of boundary layer
thickness around seagrass leaves ranging from 50
to 1000 μm depending on flow regime. Precise mea-
surements of the thickness of boundary layers around
leaves are not easily achieved, but again the mi-
croelectrode technique provides suitable means for
microscale profile descriptions and hence for mea-
surements of boundary layer thickness under stan-
dardized conditions. By inserting microelectrodes
through the leaf and out into the boundary layer,
the extension and dynamics of the DBL can be de-
scribed without disturbance caused by the electrode
tip itself (Glud et al., 1994). Unpublished data from
leaves of eelgrass exhibited DBL thickness ranging
from 140 to 440 μm at water flow velocities be-
tween 11.2 and 0.3 cm s−1(Fig. 3; Peter Larsen,
unpublished).
The rates of passive oxygen influx calculated from
the data in Fig. 3, and assuming a diffusion coeffi-
cient of 2 ×10−9m2s−1, ranged between 0.22 and
0.26 μmol O2dm−2min−1. These rates are 10–30%
of reported rates of photosynthetic oxygen evolu-
tion in eelgrass leaves (Touchette and Burkholder,
2000; Larkum et al., Chapter 14) clearly reflecting
the potential importance of passive influx to leaves
as a source of oxygen. The calculated rates of oxy-
gen influx are similar and, under the experimental
260 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
Fig. 4 . Oxygen partial pressure in horizontal rhizomes of Cymod-
ocea nodosa as a function of water flowvelocity around the leaves
measured in darkness. Intact shoots were rooted in sediment and
exposed to variable flow regimes in the laboratory. Flow velocity
was measured ∼5 cm above the sediment upstream the plant.
Reduced flow results in reduced internal oxygen partial pressure
due to the increasing thickness of the diffusive boundary layer
around the leaves (Binzer, Borum and Pedersen, unpublished.).
conditions with isolated leaves, represent an esti-
mate of leaf respiration which is independent of the
DBL thickness and the lacunal oxygen partial pres-
sure, at least if oxygen partial pressure is not very
low.
The overall effect of reduced water flow and in-
creased thickness of the DBL is that the oxygen
partial pressure inside plant lacunae declines in the
dark (Fig. 4). The influence of reduced water flow on
plant oxygen status has been demonstrated for Cy-
modocea nodosa (Fig. 4). Intact shoots with rhizome
sections were exposed to different water flow veloc-
ities in the dark, and the rhizome internal oxygen
partial pressures declined systematically at flow ve-
locities below ∼7cms
−1. Consequently, problems
related to low internal oxygen contents in seagrasses
may be exacerbated in dense seagrass beds with re-
duced flow or if flow velocities decline in very calm
weather.
The presence of epiphyte communities on sub-
merged plants may further expand the diffusive
boundary layer around leaves. The DBL-thickness
may increase to several millimeters corresponding
to a factor of 5 or more (Sand-Jensen et al., 1985).
Therefore, apart from the direct effect of epiphyte
activity on oxygen conditions immediately around
leaves, the physical presence of the epiphytic com-
munity may reduce oxygen influx to less than 20% of
that in leaves free of epiphytes. Taking the metabolic
activity of the epiphytes into account, consequences
for the oxygen balance of leaves and whole plants
may be much more pronounced. Sand-Jensen et al.
(1985) showed that the oxygen partial pressure in
epiphyte communities on leaves of submerged plants
could vary from 0 kPa in the dark to more than
45 kPa (i.e. >2 times atmospheric saturation) in the
light. Hence, the metabolic activity of dense epiphyte
communities may completely disrupt the supply of
water column oxygen to leaves during darkness and
substantially impede oxygen release from the leaves
during periods of high leaf photosynthesis. Epiphyte
density on seagrass leaves increases as a function of
nutrient richness (Borum, 1985), so eutrophication
can severely impair growth conditions of seagrasses
by epiphytes creating not only a barrier to light and
inorganic carbon but also to oxygen diffusion (Sand-
Jensen, 1977; Sand-Jensen et al., 1985).
IV. Oxygen Sinks
Oxygen is lost from seagrasses by respiratory con-
sumption, by release to the water column and by
loss of oxygen to the sediment (Fig. 5). In the light,
the respiratory oxygen consumption is supported by
oxygen produced within the leaves while oxygen is
supplied from the water column during darkness (see
Fig. 4; Larkum et al., Chapter 14). Oxygen is only
lost from leaves to the water column during the day,
when the oxygen content within the leaves exceeds
concentrations in the water, while oxygen is contin-
uously lost from roots and rhizomes to the sediment
both in the light and during darkness.
A. Oxygen Loss by Respiration
Plant respiration represents a significant loss of inter-
nal oxygen. While the majority of oxygen is lost by
diffusion to the water column and sediment during
periods of high net photosynthesis, during periods
of low photosynthesis or darkness the major sink for
oxygen is respiration. However, it is difficult to es-
timate the exact loss of oxygen in proportion to the
overall oxygen balance of the plants because several
loss processes, compartments and driving forces are
involved.
Dark respiration of leaves has been determined
for several seagrass species (e.g. Larkum et al.,
1989; Hemminga and Duarte, 2000; Touchette and
Chapter 10 Oxygen Movement in Seagrasses 261
Fig. 5 . Schematic representation of the oxygen sinks for seagrasses. Oxygen is continuously lost by respiratory oxygen consumption
in leaves, rhizomes, and roots. In the light, oxygen produced by photosynthesis is also lost by bubble formation or by diffusion to the
water column. Oxygen is continuously lost from roots and rhizomes to the reducing sediment. Oxygen levels across leaf surface and
DBL, in the light, and root surface are graphically represented; dashed lines indicate the limit of the diffusive boundary layer (see text).
Burkholder, 2000; Larkum et al., Chapter 14), and
there are no major methodological obstacles in as-
sessing these rates. In eelgrass and other seagrass
species leaf respiration ranges from 10 to 30% of
maximum photosynthetic rates (Drew, 1979; Caf-
frey and Kemp, 1991). Weight specific rates of res-
piration in below-ground tissues are significantly
lower than in leaves reflecting lower metabolic
activity (Marsh et al., 1986; Caffrey and Kemp,
1991).
The influence of high temperature on rates of res-
piration constitutes a problem of potentially large
importance for the oxygen balance of submerged
plants. Respiration seems to increase faster than
photosynthesis with increasing temperature (Marsh
et al., 1986; Masini et al., 1995; Masini and Man-
ning, 1997) and, in contrast to photosynthesis, which
exhibits optimum rates at moderate temperatures,
respiration continues to increase up to high temper-
atures. The effect of increasing respiration above an
optimum temperature is, that the oxygen content of
the shoots declines dramatically at high tempera-
tures, and plant tissues may turn anoxic even in the
light (Greve et al., 2003). At less extreme temper-
atures, the strength of the respiratory oxygen sink
may become so high, that the transport of oxygen to
below-ground tissues is insufficient to maintain aero-
bic respiration and radial oxygen loss to the sediment
(Caffrey and Kemp, 1991). This situation represents
a threat to plant survival, because toxic anaerobic
metabolites (ethanol, lactic acid, etc.) may accumu-
late within roots and rhizomes (Pregnall et al., 1984;
Smith et al., 1984).
B. Oxygen Loss to the Water Column
Oxygen is lost from the leaves to the water col-
umn during the day when the oxygen partial pres-
sure within the leaves, produced by photosynthesis,
exceeds the oxygen partial pressure of the water col-
umn surrounding the leaves. The oxygen may ei-
ther be lost by passive diffusion through the DBL or
by bubble formation on the leaves. Pressurization of
fully submerged macrophytes has been described for
Egeria densa attaining lacunal gas pressures up to 25
kPa above atmospheric pressure (Angelstein, 1910;
Sorrell and Dromgoole, 1988). The pressurization
can result in bubble formation at leaf tips, but bub-
bles can also be formed on leaf surfaces as a result of
oxygen loss by diffusion across the leaf epidermis.
Under calm, warm conditions the release of oxy-
gen into the diffusive boundary layer around leaves
may increase local oxygen concentrations above the
solubility in water. Bubble formation is, however,
less important when the water flow around leaves is
high enough to reduce the thickness of the boundary
layer and lower the pressurization within the leaves
(Sorrell and Dromgoole, 1988).
The relative importance for the overall oxygen
balance of seagrasses, of the oxygen lost from leaves
to the water column, probably varies substantially
with plant morphology (biomass/area of leaves vs.
262 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
01234
Distance behind root tip (cm)
0
20
40
60
80
100
Radial O2 loss
(ng cm-2 root surface min -1)
Fig. 6 . Radial oxygen loss from roots of Halophila ovalis as a function of distance from the root tip (n=5±SE). Relatively low
permeability of older parts of the roots prevents oxygen from being lost to the sediment before reaching the young and actively growing
root tips (Redrawn from Connell et al., 1999).
below-ground tissues) and with strength of respi-
ratory sinks within the plants and sediment. Split
chamber experiments with Zostera marina have
suggested that most of the oxygen produced by
photosynthesis escapes to the water column (Sand-
Jensen et al., 1982; Kemp and Murray, 1986; Caffrey
and Kemp, 1991), in agreement with theoretical pre-
dictions (Larkum et al., 1989). However, the absolute
rates of oxygen loss to the water column may be sub-
stantially biased by experimental conditions (Sorrell
and Armstrong, 1994) and are highly dependent on
plant species and the permeability of leaves (Sand-
Jensen et al., 1982).
C. Oxygen Loss to the Rhizosphere
Oxygen loss to the rhizosphere of submerged plants
will similarly vary with plant morphology, but a
significant loss of oxygen to the sediment from
roots of wetland and submerged plants is inevitable
(Armstrong et al., 1994). Meristems in root tips must
be supplied with sufficient oxygen to support mito-
sis and efficient energy utilization (Armstrong, 1979;
Crawford and Braendle, 1996). To ensure sufficient
oxygen supply along the length of roots to the root
apex, the radial loss from root surfaces of seagrasses
and other aquatic plants seems to decline substan-
tially with increasing distance to root tips (Fig. 6;
Armstrong, 1971; Connell et al., 1999; Armstrong
et al., 2000; McDonald et al., 2002). However, it is
likely that the radial loss of oxygen from root sur-
faces to the rhizosphere is vital to protect root tis-
sues by oxidizing reduced phytotoxins such as Mn2+,
Fe2+and sulfide (Mendelssohn and Postek, 1982;
Armstrong et al., 1996; Lee et al., 1999; Marb´a et al.,
Chapter 6, section III.E).
The proportion of oxygen lost to the sediment
is difficult to estimate precisely. A comparison of
oxygen release from roots of different submerged
aquatic macrophytes have documented the high vari-
ability among species ranging from about 1% to
100% of total oxygen release in the light (Sand-
Jensen et al., 1982). Caffrey and Kemp (1991) found
that about 10% of the oxygen produced by photosyn-
thesis in Z. marina was released by below-ground tis-
sues, but these estimates could be too low because
measurements were conducted with the roots and
rhizomes in non-reducing media and therefore with
less steep concentration gradients between plants
and media than are likely to occur in nature. Also,
oxygen release from roots, expressed as a propor-
tion of photosynthetic oxygen evolution, is a rather
confusing expression, since it implies that all oxy-
gen released originates from plant photosynthesis,
which is not the case. The oxygen released to the
sediment in the light is produced by leaf photosyn-
thesis, but oxygen lost to the sediment in darkness
originates from the water column.
There is no doubt that the oxygen released from
roots to rhizospheres of submerged macrophytes can
Chapter 10 Oxygen Movement in Seagrasses 263
Fig. 7 . Schematic representation of the internal transport of oxygen in seagrasses. The transport is basically unidirectional from the high
oxygen partial pressures in leaves or surrounding water to the low partial pressures in rhizomes, roots and sediment.
contribute significantly to aerobic mineralization of
organic matter within the sediments (Sand-Jensen
et al., 1982). For the tropical seagrass, Cymodocea
rotundata, the estimated amount of oxygen released
to the sediment was about the same magnitude as
oxygen transported from the water column to surface
sediments (Pedersen et al., 1998, 1999). Accord-
ingly, the oxygen loss to sediments has important im-
plications for the degradation of organic matter but
potentially also for other redox processes such as sul-
phide reoxidation (Lee and Dunton, 2000) and cou-
pled nitrification–denitrification (Caffrey and Kemp,
1992). By leaking oxygen from the roots at different
rates during light and dark periods, the rhizosphere
immediately around roots of aquatic plants experi-
ences fluctuating aerobic and anaerobic conditions
which may promote denitrification (Christensen and
Sørensen, 1986; Caffrey and Kemp, 1990; Caffrey
and Kemp, 1992; Flindt, 1994). However, in situ ob-
servations of coupled nitrification–denitrification in
beds of Zostera marina and Z. noltii have not demon-
strated higher rates than in bare sediments (Rysgaard
et al., 1996; Risgaard et al., 1998), so there is a need
for more detailed analysis of the complex interac-
tions between plant oxygen release and sediment
processes (see also Marb´a et al., Chapter 6).
V. Internal Movement of Oxygen
A. General Characteristics
The internal transport of oxygen in seagrasses is pre-
dominantly unidirectional from leaves to rhizomes
to roots driven by the gradient between high oxygen
partial pressures in leaves or water and low partial
pressures in roots and sediment (Fig. 7). Seagrasses
have well-developed lacunae in leaves, rhizomes and
roots with tissue porosities up to 30% or even more
(Penhale and Wetzel, 1983; Larkum et al., 1989). The
leaf lacunae are connected to the rhizome lacunae
(Kuo et al., 1981; Kuo and Den Hartog, Chapter 3);
there are often diaphragms at the nodes and transition
regions, but these offer little resistance to gaseous
diffusion (Larkum et al., 1982). From the rhizome,
lacunae continue into each root. Oxygen transport
to the most distal, newly formed root tips, however,
relies on liquid phase diffusion over short distances
(Armstrong, 1979; Colmer, 2003). The formation
of air-spaces within below-ground tissues seems to
be stimulated by ethylene produced under conditions
with low internal oxygen contents (Drew et al., 2000;
Colmer, 2003), and lacunal development in eelgrass
has been shown to increase with higher sediment or-
ganic content and lower redox potential (Penhale and
Wetzel, 1983).
B. Oxygen Transport by Diffusion
Gas transport within the majority of emergent and
submerged aquatic plants is believed to be driven
primarily by diffusion rather than by convective
flow (Armstrong, 1979; Sorrell and Dromgoole,
1987; Larkum et al., 1989). Passive gas phase
diffusion within seagrasses occurs continuously
along the downhill partial pressure gradients from
leaves to rhizomes to roots. In the light, the high
264 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
0 25 50 75 100 125 150
Time (min)
pO2, meristem (kPa)
Light Dark
Air saturation
10
20
30
40
0
Fig. 8 . Changes in oxygen partial pressure in meristematic tis-
sues of an intact eelgrass shoot during a light–dark transition
experiment. The rapid (∼45 min) establishment of a low steady
state oxygen partial pressure in the dark strongly suggests that
rates of oxygen transport between tissues and losses to respira-
tion and external media are high (Redrawn from Greve et al.,
2003).
oxygen partial pressure in leaves generated by
photosynthesis create steep gradients from leaves to
water column and less steep gradients from leaves to
below-ground tissues. During darkness, the oxygen
partial pressure in leaves declines below that of
the water column, and the oxygen flux becomes
directed from water to leaf, instead of vice versa
(Greve et al., 2003). Although weaker than in the
light, the gradient from leaf to rhizomes and roots
persists during darkness ensuring a continuous
supply to below-ground tissues.
Rapid changes in the oxygen content of meris-
tematic tissues in the transition between leaves and
rhizomes of eelgrass suggest that rates of internal
oxygen transport and losses to the external media
are high and that internal oxygen pools are rela-
tively short-lived (Fig. 8; Greve et al., 2003). A thor-
ough examination of oxygen losses in the submerged
freshwater macrophyte Egeria densa (Sorrell and
Dromgoole, 1987, 1988) showed that internal pools
of oxygen were depleted rather slowly (up to 4 h)
probably due to high resistance toward gas exchange
between leaves and water column. Seagrasses may
have more gas permeable leaves because time in-
tervals between the occurrence of new steady state
oxygen balances in both Zostera marina (Fig. 9;
Greve et al., 2003) and Cymodocea rotundata (Ped-
ersen et al., 1998) were less than 2 h after light–dark
switches. One consequence of this apparently high
permeability is that the internal pool of oxygen built
up by photosynthesis during the day is insufficient
to support night-time respiration of leaves, rhizomes
and roots, in contrast to what is often supposed (e.g.
Smith et al., 1984; Touchette and Burkholder, 2000).
Rapid internal transport of oxygen by passive dif-
fusion from the leaves of Zostera marina to the
meristematic region and further on to rhizome in-
ternodes is also demonstrated by changes in internal
oxygen partial pressures after manipulation of water
column oxygen concentrations during darkness (Fig.
9A). Water column oxygen was lowered stepwise
from atmospheric equilibrium to zero, and after each
step, new steady-state oxygen partial pressures were
rapidly attained within the meristematic tissue and
at two positions along the rhizome. An oxygen gra-
dient persisted throughout the experiment with the
highest oxygen partial pressure in the meristematic
region and the lowest in the oldest rhizome intern-
ode. At a water column oxygen partial pressure cor-
responding to about 25% of air saturation the most
distal rhizome internode became close to anoxic, but
traces of oxygen were still observed in rhizome in-
ternode #3 and in the meristematic tissue reflecting a
continuous transport of oxygen by passive diffusion.
The experiment with stepwise reduction in wa-
ter column oxygen concentrations makes it possible
to estimate the velocity of internal oxygen transport
within the rhizome of Zostera marina (Fig. 9B). For
each step, there was a consistent lag period between
the time when water column oxygen had started to
decline until changes in the oxygen partial pressures
within the rhizome sections were recorded. The dis-
tance between the meristematic region and rhizome
internode #4 was about 5 cm, and the traveling time
for oxygen over that distance was 4–5 min clearly
reflecting rapid gas phase diffusion.
C. Oxygen Transport by Mass Flow
Mass flow of lacunal gasses has been demonstrated
for several emergent plants (Dacey, 1981; Armstrong
and Armstrong, 1990; Brix et al., 1992), but ma-
jor oxygen transport by mass flow likely requires
through-flow provided by tissue contact with the at-
mosphere. In submerged plants, mass flow could
theoretically occur on a small scale driven by in-
ternal pressurization generated from photosynthesis
or by leaf movement due to waves or water current.
However, gas phase diffusion should be sufficient
to ensure oxygen transport in submerged plants as
Chapter 10 Oxygen Movement in Seagrasses 265
Fig. 9 . (A) Internal oxygen partial pressure in eelgrass tissues as a function of water column oxygen content. The rapid establishment
of steady states inside the tissues reflects the efficiency of internal oxygen transport by passive diffusion. (B) Relative changes in
oxygen concentrations of the water column, the eelgrass meristem and of rhizome internodes #3 and #4 upon stepwise reduction of
water column oxygen concentration. The lag period between changes in oxygen concentrations of the different tissues reflect traveling
velocities within the lacunae of the rhizome. The distance between the meristematic tissue and internode #4 was about 5 cm (Pedersen,
Borum and Binzer, unpublished).
convincingly argued by Sorrell and Dromgoole
(1987, 1988).
Pressurization does take place in submerged
plants (Sorrell and Dromgoole, 1987) and has also
been observed in seagrasses (Roberts and Moriarty,
1987; Terrados et al., 1999). In the light, lacunal
gas pressure above atmospheric pressure was built
up in the horizontal rhizome of the Mediterranean
seagrass, Cymodocea nodosa (Fig. 10). In a young
rhizome internode lacunal gas pressure stabilized at
around 15 kPa above atmospheric pressure. In an
older internode of the same plant, steady state gas
pressure in the light was consistently lower reflect-
ing the existence of the internal pressure gradient,
which is required to drive any mass flow. In the
dark, lacunal gas pressure quickly fell to levels be-
low atmospheric pressure and an inverse pressure
gradient from the older to the young rhizome intern-
ode was established (Fig. 10). The pressure gradient
could potentially generate a mass flow of oxygen
from the young to the older internode in the light
and thereby supplement diffusive oxygen transport
to below-ground tissues, while in darkness, a pos-
sible mass flow would counteract diffusive oxygen
transport to the roots. The existence of pressuriza-
tion and pressure gradients does not reveal much
about the importance of mass flow for internal oxy-
gen transport. Relatively strong gradients may be
formed with little mass flow, if the resistance to mass
flow by the diaphragms/septa, regularly interrupting
seagrass lacunae to prevent flooding (see section V
A), is high. On the other hand, mass flow could play a
role in gas transport under transient conditions with
shifts from the dark to light and if leaf movements
generate variable pressures within the leaves. These
aspects deserve further investigation.
VI. In Situ Oxygen Variability in Seagrass
By use of microelectrodes, diel changes in the
internal oxygen partial pressure of both Zostera
266 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
0 50 100 150 200 250 300
Time (min)
80
90
100
110
120
130
Lacunal gas pressure (kPa)
Internode 1
Internode 5
Light Darkness
Fig. 10. Internal gas pressure in rhizome internodes of Cymod-
ocea nodosa during a dark–light-dark transition experiment. In
the light, gas pressures above atmospheric pressure were build up
and a steady state pressure gradient occurred between the young
rhizome internode #1 and the older internode #5. In the dark, an
inverse gradient was formed at sub-atmospheric pressures (Re-
drawn from Terrados et al., 1999).
marina (Fig. 11; Greve et al., 2003) and Thalassia
testudinum (Borum et al., 2005) have been assessed
in situ under different environmental conditions. The
oxygen content of eelgrass meristems followed sim-
ilar temporal patterns and varied substantially over a
diel cycle (Fig. 11). Internal oxygen partial pressures
Fig. 11. Diel changes in surface irradiance and oxygen partial pressures of the water column and meristematic tissues of three eelgrass
shoots measured in situ. During daylight, the fluctuating internal oxygen contents are intimately coupled to surface irradiance, while at
night, changes in water column oxygen concentration seem to be the most important forcing factor controlling internal oxygen partial
pressures (Borum, Pedersen and Binzer, unpublished).
were above water column oxygen partial pressures
and above atmospheric equilibrium in the afternoon
at high surface irradiances and fluctuated systemati-
cally with changes in irradiance the following morn-
ing. In the dark, internal oxygen partial pressures de-
clined steadily to low levels of about 15% of atmo-
spheric equilibrium around sunrise. Similar patterns
in plant oxygen contents have been recorded during
other diel measurements on stands of Zostera marina
(Borum, Pedersen and Binzer, unpublished) and of
Thalassia testudinum (Borum et al., 2005).
As suggested from Fig. 11, oxygen partial pres-
sures within the plants seem primarily dependent
on changes in surface irradiance in the light and
controlled by changes in water column oxygen con-
centrations at night. This suggestion is confirmed
when internal oxygen partial pressures are plotted
vs. surface irradiance in the light (Fig. 12A) and wa-
ter column oxygen in the dark (Fig. 12B). In the light,
the relationship resembles a typical photosynthesis–
irradiance curve with increasing internal oxygen
contents at low light reaching saturation at high light,
while in the dark, plant oxygen contents are linearly
related to the oxygen concentration in the water col-
umn. The oxygen content at high light is determined
by the balance between the light-saturated oxygen
evolution in leaves and the oxygen losses due to
plant respiration and the oxygen efflux to the water
Chapter 10 Oxygen Movement in Seagrasses 267
Fig. 12. Plant oxygen partial pressures from Fig. 11 plotted (A)
vs. surface irradiance (data from afternoon), and (B) versus wa-
ter column oxygen partial pressure for the dark period (Borum,
Pedersen and Binzer, unpublished).
column and sediment. The baseline oxygen partial
pressure at zero irradiance (Fig. 12A) and the linear
relationship between plant and water column oxygen
in the dark (Fig. 12B) are determined by the balance
between oxygen supply from the water column and
oxygen losses due to plant respiration and the oxy-
gen efflux to the sediment.
In the tropical turtle grass in Florida Bay, diel
changes in internal oxygen content, similar to those
shown in Fig. 11, have been recorded at several sites.
Here, internal plant content of oxygen varied not
only with surface irradiance and water column oxy-
gen but also with sediment composition and plant
density (Borum et al., 2005). In a sparsely vege-
tated bed with a moderate content of organic mat-
ter in the sediment, the oxygen partial pressure in
the meristematic tissues remained relatively high
throughout the diel cycle, while in a dense stand with
organically rich sediments, the meristematic tissues
turned anoxic during darkness, and rhizome and root
metabolism had to rely on anaerobic metabolism for
several hours during the night. These observations
suggest that the oxygen partial pressure inside these
tropical seagrasses is significantly influenced by re-
duced oxygen supply from the water due to lower
water flow velocity in dense seagrass stands and/or
by higher oxygen losses due to higher respiratory
oxygen demands of more organically rich sediments,
at higher temperatures compared to temperate sea-
grasses.
VII. Anoxia and Seagrass Die-off
Insufficient oxygen supply to meristems and roots
of seagrasses may have severe implications for sea-
grass growth and survival. Tissue anoxia impairs
growth of roots, nutrient uptake and translocation
of nutrients and carbohydrates (Smith et al., 1988;
Zimmerman and Alberte, 1996), and the disappear-
ance of the oxic microshield around roots and rhi-
zomes normally provided by the radial oxygen loss
allows the invasion of reduced phytotoxins from
the sediment to the plant tissues. Periodical inva-
sion of sulfide from the sediment into roots of wet-
land plants has been indicated by the composition
of sulfur isotopes in the roots (Carlson and Forrest,
1982; see also Koch et al., Chapter 8), and inva-
sion of gaseous sulfide into seagrass lacunae has
been measured using microelectrodes both under
laboratory and field conditions for Zostera marina
and Thalassia testudinum (Pedersen et al., 2004;
Borum et al., 2005). It is not known whether the
events of sudden seagrass die-off, which have been
reported for temperate and tropical seagrass beds
(Robblee et al., 1991; Greve et al., 2003), are caused
by poor energy availability during anaerobiosis, by
accumulation of toxic plant metabolites or by inva-
sion of toxic compounds from the sediment. All these
phenomena, however, seem to originate from an in-
sufficient supply of oxygen from leaves to the meris-
tematic tissues or below-ground tissues. To reach a
clearer understanding of the reasons for sudden sea-
grass die-offs, it is important to examine rates and
mechanisms of oxygen transport in seagrasses fur-
ther and to establish more direct links between oxy-
gen dynamics and plant mortality (see also Koch
et al., Chapter 8).
VIII. Summary
Measurements of oxygen variability and transport in
seagrasses and other submerged plants are difficult
268 Jens Borum, Kaj Sand-Jensen, Thomas Binzer, Ole Pedersen and Tina Maria Greve
to conduct and interpret due to the existence of sev-
eral sources and sinks of oxygen driving internal
transport at different rates depending on conditions
in the water column and sediment. Oxygen release
and transport in seagrasses have mostly been as-
sessed by measuring oxygen changes in incubation
chambers, but oxygen variability within the plants
can be assessed at much higher spatial and temporal
resolution using microelectrodes. Also planar op-
todes could be applied to describe oxygen release
to the rhizosphere at higher spatial and temporal
resolution.
Quantitatively, photosynthetic oxygen evolution
is the most important source of oxygen for internal
transport and aerobic metabolism, but passive dif-
fusion of oxygen from the water column to leaves
and below-ground tissues during darkness is also
important, and this source is necessary for maintain-
ing the oxygen supply to roots and rhizomes during
dark periods of more than 1–2 h. The largest loss
of oxygen from seagrasses is from leaves to water
column during periods of high light and photosyn-
thesis, but the continuous leakage of oxygen from
roots and rhizomes to the anoxic sediment both dur-
ing light and dark periods also represents a major
sink to plant oxygen. During high photosynthesis
and active plant growth, the respiratory oxygen con-
sumption is much lower than oxygen release to the
external media. However, the relative importance
of respiration increases markedly with increasing
temperature or at times of low photosynthetic rates.
The internal transport of oxygen between leaves and
below-ground tissues is most likely to be primarily
driven by passive diffusion within the air-filled lacu-
nae. Pressurization, however, does occur and may ac-
count for some internal oxygen transport especially
during transient shifts between light and darkness.
There is a need for more direct measurements of
oxygen traveling velocities to elucidate the roles of
passive diffusion vs. pressurization under different
environmental conditions, and the possible coupling
between internal oxygen dynamics and seagrass die-
offs deserves further investigation.
Acknowledgments
This work has been partially funded by the EU
(EVK3-CT-2000-00044) and the Danish Research
Agency (&41-00-49.66). We thank Peter Larsen for
allowing us to present unpublished data on the thick-
ness of diffusive boundary layers. We wish to thank
the reviewers, W. Armstrong, W.M. Kemp and B.
Sorrell, for their helpful comments and valuable sug-
gestions.
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