Marine Biology73, 37-42 (1983)
Marine
=,=BiOlOgy
9 Springer-Verlag 1983
Release of Dissolved Organic Carbon from the Estuarine Intertidal Macroalga
Enteromorphaprolifera
A. M. Pregnall
Oregon Institute of Marine Biology; Charleston, Oregon 97420, USA
Abstract
The estuarine macroalga Enleromorpha prolifera was collected from Coos Bay, Oregon, USA during 1981, and its release
of photosynthate as dissolved organic carbon (DOC) was
studied using 14C as a tracer. During photosynthesis in
30%0 S sea water, with a fixation rate averaging 7.37 mg C
g-1 dry wth-~, release ranged from 0.13 to 0.57mgC
g-~ dry w t h -~ and from 1.65 to 6.23% of total fixed
carbon. Release of DOC appears to be linear with time
over 3 h. As exposed algae become increasingly desiccated,
their photosynthetic rates decline dramatically, but upon
reimmersion the highly desiccated algae lose a larger
fraction of their fixed carbon than the slightly desiccated
algae. This loss comes in a pulse release of DOC over the
initial 15 rain, followed by declining release rates. The
pulse loss due to rainfall is 5 times greater than that due to
9tidal resubmergence, and may briefly exceed the prior
photosynthetic rate. Although lowering the salinity from
30 to 5%0 does not substantially alter photosynthetic
rates, it does increase the DOC release range up to
1 . 0 2 m g C g - l d r y w t h -~ and 16.10% of fixed carbon.
Heterotrophic microbes from the algal habitat readily use
the available DOC at about 15% h -a.
Introduction
Marine macrophytes photosynthetically fix large quantities of carbon into organic substances. While it is assumed
that most of this material becomes available to the aquatic
community as particulate detritus some time after synthesis (Odum and de la Cruz, 1967), much of it enters the
environment as dissolved organic carbon (DOC) both
during photosynthesis and following senescence (Khailov
and Burlakova, 1969; Sieburth, 1969; Moebus and Johnson, 1974; Brylinsky, 1977).
Most of the DOC released during photosynthesis appears to consist of relatively small organic molecules,
which are likely to be metabolic intermediates (Wetzel
and Manny, 1972; Sondergaard, 1981). The abundant
heterotrophic microbes in natural habitats readily utilize
these substances by assimilation and respiration (Nalewajko and Lean, 1972; Bauld and Brock, 1974; Williams
and Yentsch, 1976; Brylinsky, 1977)9
The macrophyte assemblages of major importance in
estuaries are usually the salt marshes and seagrass beds
(Correll, 1978), both of which have been found to release
DOC (Gallagher et al., 1976; Penhale and Smith, 1977).
The estuary of Coos Bay, Oregon, USA has very little salt
marsh remaining (Hoffnagle and Olson, 1974), but does
have many large eelgrass beds. However, from 10 to 70%
of the standing crop of these eelgrass beds consist of the
associated green algae (Gonor et al., 1979), Additionally,
the numerous intertidal flats support seasonally abundant
populations of macroalgae, primarily of Enteromorpha
spp. (Chlorophycophyta: Ulvales). The two major species
are E. ?rolifera, a long, profusely branching, filamentous
form, and E. linza, a flat, sheet-like form. Both species
maintain high photosynthetic rates while submerged (King
and Schramm, 1976; Littler and Littler, 1980).
The intertidal habitat of Enteromorpha spp. mats in
Coos Bay subjects them to the typical fluctuations of
repeated exposure and resubmergence, potential desiccation and rainfall stress, and variable estuarine salinity.
These factors affect photosynthetic rates and DOC release
in some marine macrophytes (Sieburth, 1969; Johnson
et al., 1974; Moebus et al., 1974; Penhale and Smith, 1977;
Quadir et aI., 1979; Gordon et al., 1980). The purposes of
the present study were to quantify the release of DOC
from actively photosynthesizing thalli of E. ?rolifera, with
particular attention to the above-mentioned environmental
fluctuations, and to investigate the potential for use of this
DOC by heterotrophic microbes.
Materials and Methods
Samples of Enteromorpha prolifera were collected from
mudflats in the South Slough arm of Coos Bay, Oregon,
A.M. Pregnall: DOC Release from Enteromorpha
38
USA at +2.0 ft (0.6 m above mean lower low water,
MLLW) during August-October, 1981. Thalli were
gently rinsed in sea water to remove sediments, small
grazers, and epiphytes, and then held overnight in aerated,
ambient-temperature sea-water aquaria.
For determinations of photosynthetic rates and DOC
release rates, algae were incubated in either 300 ml bottles
or 1.5-liter Plexiglas chambers with magnetic stir bars.
Each Plexiglas chamber had two stoppers through which
fluids could be injected or withdrawn by syringe and an
insert grid to which the algae were attached.
Gently blotted algae of known fresh weight were
placed in the incubation vessels, and sterilized synthetic
sea water (Rila Sea Salts) of the required salinity was then
added. The dissolved carbon dioxide, bicarbonate, and
carbonate concentrations of the water were determined
beforehand using the techniques of Strickland and Parsons
(1968). The average algal density over all experiments was
0.29 g dry wt 1-1. Bottles and chambers were maintained
at 16~ in a water bath. 20ffCi of NaH14CO3 (New England Nuclear) in 1 ml was added to the 1.5-liter chambers,
and 4~Ci to the 300ml bottles, with a final specific
activity of about 0.82/~Ci mg -~ dissolved inorganic carbon. All incubations were performed outside between
11.00 and 15.00hrs on clear, sunny days in early fall to
ensure that light intensities would be above saturation
(King and Schramm, 1976). Dark controls were wrapped
in foil, and samples were taken just after the introduction
of label to establish initial background activities.
At the end of the 3 h incubation, algae were fixed for
1 h in 100 ml of 5% formalin in 30%0 S sea water adjusted
to pH 2.0 with HC1. Following dry weight determination,
the algae were ground to a fine powder, and the activities
of aliquots of 10 to 30 mg were counted by liquid scintillation. Aliquots of the algal fixative were also counted, for
some activity leached from the algae. Each sample was
counted 3 times for either 15 min or to 1.5% accuracy on a
Beckman LS 150 Scintillation Counter. Corrections for
quench were made using standard curves of percent
counting efficiency versus external standards ratio.
At specified intervals during the incubations, 3 ml
water samples were removed from the vessels and acidifled to pH 2 in scintillation vials with 0.5 ml of the algal
fixative described above. These were then flushed for
10 min with CO2-free air. Controls indicated that less than
0.1% of inorganic label remained after flushing. The
resulting acid-stable ~4C activity is the experimental measure of DOC.
Desiccation of exposed algae was determined by placing variable amounts of fresh algae in 100X 15 mm petri
dishes with a known weight of water-saturated sediment
covering the bottom. The uncovered dishes were positioned in a random grid and placed outside in the late
morning. At time intervals up to a total desiccation
duration of 3 h, the total weights of algae, sediment, and
dish, and of just sediment and dish were measured. Dry
weights of algae and sediments were determined after
overnight drying in a 90 ~ C oven.
For measurements of photosynthesis in air, a modification of the procedure of Darley etal. (1976) was used.
Desiccated algal sections were placed in the 1.5-liter
chambers with 20 ktCi of tracer in 1 ml in a cup, after
which the chambers were equilibrated in the water bath,
sealed, and ~4CO2 liberated by the addition of I ml of 85%
lactic acid to the cup. After 20 min, the algal pieces were
removed and subdivided. One half of each section was
fixed, and carbon uptake was determined as before. The
other half was immersed in 100 ml synthetic sea water for
1 h, and DOC release was measured.
Results
In seven 3 h incubations of Enteromorpha prolifera samples in 30%0 S sea water, net carbon fixation in the light
averaged 7.37 mg C g-1 dry wt h -1, and DOC release
averaged 0.26 mg C g-1 dry wt h -1, giving a mean of 3.5%
of recently fixed carbon lost (Table 1). Dark fixation and
release rates were both less than 1% of the light rates.
Fig. 1 shows the time course of the accumulation of DOC
for one of the incubations. Over the 3 h of the experiment,
DOC accumulation appeared to be linear, with a constant
release rate.
The algal mats on the mudflats in Coos Bay occur
between MLLW and +5.0ft (1.5 m), and are thus uncovered by many or all outgoing tides. As tidal patterns
and daylength change, the amount of time that these algae
spend exposed varies. The degree to which algae become
desiccated depends highly upon the duration of exposure
and upon the amount of algae present. Fig. 2 indicates the
moderating effect that increased standing crop has upon
desiccation. If the algal mat is less than about 1 cm thick,
the algae may quickly lose internal water, while above
1 cm thickness, only the surface elements of the mat
3.0
.~
Y=0.572 X+ 0.056
~,
'~
O
9
T"z= 0.79
2.0
:~
-
~
1.0
(~3
9
I
1
I
2
I
3
TI ME (HOURS)
Fig. 1. Enteromorpha prolifera. Time course of DOC release by
algae with a photosynthetic rate of 9.18 mg C g-1 dry wt h -1
A. M. Pregnall: DOC Release from Enteromorpha
39
Enleromorpha pro[ifera. Carbon fixation and dissolved
organic carbon (DOC) release rates for algae in 30%0 S sea water
Table 1.
Carbon fixation rate
(rag C g-1 dry wt h -1)
DOC release rate
(mg C g 1 dry wt h -1)
6.05
6.28
6.27
6.86
7.89
9.05
9.18
mean: 7.37_+ 1 . 3 4
I00
% DOC
Light incubation
0.13
0.21
0.31
0.2O
0.27
0.15
0.57
2.1
3.3
4.9
2.9
3.4
1,7
6.2
0.26-+0.15
3.5_ 1.6
ALGAL MAT THICKNESS (cM)
I
2
5
I
-1-
I
./
iT]
9
"
__.
I
9 9
9
- -
9
%
9
50
-r
w
u..rr"
#
;
1-'z= 0.91
_
Y : 28.618 L N ( X ) - 115.665
-
Dark incubation
0.020
0.010
0.008
mean: 0.013--+0.006
0.003
0.001
0.003
15.0
10.0
37.5
0.002-+0.001
20.8-+ 14.6
become dried to any great extent, and the lower layers
remain quite moist and capable of photosynthesis if they
are not too greatly shaded.
As the algae become increasingly desiccated, their
photosynthesis drops quickly (Fig. 3) until they are barely
fixing carbon after 50% fresh weight loss. However, when
these desiccated algae are reimmersed by the incoming
tide, they lose some of their recently fixed carbon. The
greater the fresh weight loss during drying, the greater the
fraction of their fixed carbon lost becomes (Fig. 4).
Exposed algae m a y either be submerged by the incoming tide or be subjected to rainfall. Previously labelled
algae were desiccated to 65% fresh weight, and carbon
fixation was determined from a subsample. A portion of
the algae was reimmersed in 100ml of 30%0S synthetic sea
water, and another was subjected to simulated rainfall:
100 ml fresh water was sprinkled through an inverted
Buchner funnel, and the algae allowed to remain covered
by the accumulated water. Water samples were removed
at 0, 15, 30, 60, and 180 rain after initiating reimmersion or
rainfall and analyzed for DOC. Release rates were calculated for each time interval between samplings. These
slightly desiccated algae release D O C upon reimmersion
in a rapid pulse over the first 15 to 30 rain (Fig. 5). If the
reimmersion is due to steady rainfall, the loss of D O C is
greater in both magnitude and duration; initially, the rate
of release may be greater than the prior photosynthetic
rate.
While the carbon fixation rate of Enteromorpha prolifera is slightly reduced to an average o f 5.6 mg C g-1
dry wt h -1 at lower safinities, it does not vary consistently or
greatly over the range tested here (30 to 5%o), with a
standard deviation o f only 0.66 mg C g-1 dry wt h -1
(N = 10). However, the fraction of fixed carbon that is lost
as D O C increases to about 15% at 5%0, from the more
typical 5% at 30%0 (Fig. 6). It is not known whether the
D O C release is reduced at higher salinities.
0
I
I
I
I
2000
4000
ALGAL STANDING CROP (G FRESHWT-~Z)
Fig. 2. Enteromorpha#rolifera. Degree of desiccation of exposed
algae through time as a function of standing crop after l h
(dashed line) and after 3 h (continuous line). Plotted points and
regression eqtlation are for t = 3 h
e-
<
o
2.0-
r
~-.
_'T
z~
=-0.8604
, p z : 0.99
+
\
\
LN(X) + 5.7056
c~ 1.0 -
O~
I
>-?O!
n
O
I
9
L9
40
80
% FRESH WEIGHT LOSS
Fig. 3. Enteromorphaprolifera. Photosynthesis in air by algae as
a function of increasing desiccation
tad
~
0
0
r'~
,,=, 6o-
03
<
....I
.2
<
__J
m
4O-
ct
20 -
L<
I
-
-pa : 0.84
~
/
Y= 0.7o42 X - 0.2225
0|/ 9
0
l
i
~
i
40
80
% FRESH WEIGHT LOSS
Fig. 4. Enteromorpha prolifera. Release of previously fixed labelled carbon during 1 h following reimmersion of desiccated
algae in sea water
A.M. Pregnall: DOC Release from Enteromorpha
40
Z
O
1213
cr
10
<
o
a
T-,- Q 6 -
-1'
i
I
i
.I,
E. PROLIFERA
r.~
9
Lt.ll~
9 E. LiNZA _ ___.
9
~,,~
<17
cc 0.4
>....
_.1
z
0
0
r,...)
o3 5
§
>
Ld
cc
(3_
I,
O
I
"RAINFALL"
O3
<
W
_.1
0
o
c~
SEA WATER
L~
T
0
previously fixed carbon following reimmersion in sea water or by
simulated rainfall
in presence of sediment-associated microbes as a function of
initial concentration. Rate is hourly average over entire 5 h
incubation period
Table 2. Reduction of DOC activity in presence of microbes. Values are for 3 h incubations, dpm = disingegrations per rain
Initial
(m1-1 )
(.)
15
-
9
Sediments
922
627
942
801
792
690
976
9
~
|
9
9
Final
(m1-1 )
795
282
406
365
385
307
479
Decrease
% Decrease
(dpm m1-1)
Corrected %
(-control %)
127
345
536
436
407
383
497
control
41.2
43.1
40.6
37.6
41.7
37.1
13.8
55.0
56.9
54.4
51.4
55.5
50.9
mean: 40.2_+ 2.3
o<5
s
W
Y = - 0 . 3 3 4 X + 15.990
x
U_
I
5
Fig. 6.
I
I
I
0.6
0.8
1.0
TNITIAL DOC CONCENTRATION (MGC.C%
Fig. 7. Enteromorphaprolifera and E. linza. Rate of DOC removal
I
2
3
W
rr
TIME AFTER REIMMERSION (HOURS)
Fig. 5. Enteromorphaprolifera. Time course for rate of release of
o
0.0057
rr Q2
o
W
T"z = 0.96
Y= 0.0615 X -
W
I
I
I
~
...o'o
I
I
I0
20
SALINITY (%.)
Enteromor?ha prolifera. Percentage of
I
I
25
30
fixed carbon re-
Epiphytes
1 193
1 019
963
1 045
917
1 100
1 245
l 126
456
542
532
431
479
513
67
563
421
513
486
621
732
5.6
55.3
43.7
49.1
53.0
56.5
58.8
control
49.6
38.1
43.5
47.4
50.8
53.2
mean: 47.1 __5.5
leased as DOC for pairs of incubations at 5 salinities
The labelled m a t e r i a l that Enteromorpha prolifera
releases during short-term photosynthetic incubatioris
p r o b a b l y consists o f intermediate metabolites. The heterotrophic microbes from the algal habitat, present on the
algal thalli as epiphytes a n d in the sediments, should
prove capable o f taking up labelled D O C from sea water.
To test this, 150 ml o f water in which algae h a d been
incubating a n d releasing labelled D O C for 3 h were a d d e d
to replicate foil-wrapped bottles containing either 20 g o f
mudflat surface s e d i m e n t or 3.5 g fresh weight o f heavily
epiphytized E. prolifera. The bottles were held at 16 ~ C for
3 h and hand-swirled every 30 min to circulate the water
without stirring up the sediments. The initial a n d final
D O C concentrations were d e t e r m i n e d as above. Controls
were autoclaved sediments a n d algae. Table 2 shows the
decrease in D O C activity in the presence o f these microbes. The control reductions are likely to be due to
adhesion o f the organic molecules to particulates. Thus,
over a 3 h period, a b o u t 40% o f the available D O C was
utilized by sediment-associated microbes, and about 47%
was utilized by epiphytic microbes.
In a separate experiment, 300 ml o f D O C - c o n t a i n i n g
water from incubations with Enteromorpha prolifera a n d
from E. linza was i n c u b a t e d for 5 h with sediments. There
was a control-corrected decrease o f 75.4+5.8% o f the
D O C from E. prolifera, a n d a decrease of 71.5 4- 4.1% o f
the D O C from E. linza. The rate o f utilization appears to
increase directly with the a m o u n t o f D O C available, a n d
there is no a p p a r e n t difference in the use o f D O C by the
two different species (Fig. 7).
A. M. Pregnall: DOC Release from Enteromorpha
Discussion
Release of dissolved organic carbon from Enteromorpha
prolifera falls among the higher values reported in the
literature, particularly for studies using 14C incorporation
and release techniques (Khailov and Burlakova, 1969; Sieburth, 1969; Moebus and Johnson, 1974; Brylinsky, 1977;
Penhale and Smith, 1977); this is largely due to the high
photosynthetic rate of this alga. The DOC activity of
E. prolifera is composed of recently labelled materials, so
there may be other substances being released which have
not been detected. Thus, all values reported here are conservative. However, because of the intertidal location of
the algae, the duration of submergence in daylight and the
period of such photosynthesis may be only a few hours at
a time, so the values measured here should be realistic.
As compared to my data, the release rates reported by
Khailov and Burlakova (1969) and by Sieburth (1969) are
higher, presumably due to (1) differences in their methods
of measurement, which would detect release of materials
synthesized far prior to the time of release, and (2) the
potential injury or senescence of their algal material, as
they suggest. Moebus and Johnson (1974) found substantial loss of DOC from injured holdfasts of fucoid
algae. The potential for overestimation of normal DOC
release due to injury of Enteromorpha prolifera in the
present study is small, for only the cells at the very ends of
the thin filaments would be broken. The carbon-fixing
mechanisms of the broken cells would be disrupted, which
should reduce the incorporation of label into stable products. The slightly higher release rates for submerged
photosynthesis reported by Sieburth (1969) coupled with
the lower photosynthetic rates of his brown algae, relative
to E. prolifera, result in his much higher percent release
values of 25% compared with about 3.5% in the present
study.
The materials most likely to be released during photosynthesis would be relatively small, labile molecules such
as amino acids, sugars, organic acids, and sugar phosphates. Sondergaard (1981) determined that most of the
DOC released by the freshwater macrophyte Littorella
uniJlora has a molecular weight of approximately 200.
Wetzel and Manny (1972) determined that about 90% of
the organic matter excreted by another freshwater macrophyte, Najas flexilis, are sugars and other labile, lowmolecular-weight compounds. Fogg (1976) found measurable release of glycollate from some tropical marine
macrophytes. Patil and Joshi (1970) found a high intracellular turnover of such metabolites in Ulva lactuca, with
the ethanol-soluble activity remaining fairly constant over
several hours, while the ethanol-insoluble components continued to increase in activity. If the pool of potentially
releasable molecules is fairly constant in size, one would
expect a constant release rate, with a linear accumulation
of DOC in the incubation medium.
While some algae, particularly the high-intertidal
fucoids, increase their photosynthetic rates in air after
some desiccation (Johnson et al., 1974; Quadir et al., 1979),
41
Enteromorpha prolifera shows much reduced carbon fixation rates after as little as 30% fresh weight loss. Such a
reduction in photosynthesis is typical for algae with very
thin thalli (Imada et al., 1970; Johnson et al., 1974; Wiltens et al., 1978; Quadir et al., 1979).
The observations that increased desiccation of algae
results in an increased fraction of fixed carbon lost upon
reimmersion and that the release comes in a pulse over the
first 15 rain suggest that moderate desiccation can be quite
stressful to the cellular stability of Enteromorpha prolifera.
The increased magnitude and duration of DOC release
indicate that rainfall on exposed algae is another severe
stress. These increases are likely to be due to the influence
of reduced salinities as well as the shock of resubmergence.
It is possible that the organics released following reimmersion under stressful conditions include not only the
smaller metabolites presumed for typical submerged
release, but also larger, more complex substances such as
polypeptides and structural carbohydrates released by cellwall damage. Such damage could well result in a large but
brief pulse release after reimmersion.
Sieburth (1969) found reduced DOC release with lower
salinities in fucoid algae and suggested that it was due to
lowered photosynthetic rates. The total carbon fixation
rate of Enteromorpha prolifera was not reduced with decreased salinity in the present study, and DOC release increased at lower salinities; thus the release is probably
passive and may be affected by the osmotic relation between the cells and the surrounding medium.
All of the typical estuarine fluctuations in this study of
Enteromorpha prolifera increased the rate of DOC release
and/or the fraction of fixed carbon released. This indicates
that field populations of the algae are repeatedly confronted with a variety of stresses, and that the fragile
structure of these green algae (relative to that of the fucoids
or laminarians, for example) provides little protection.
They are thus able to achieve standing crop levels of 100
to 350 g dry wt m ~ over a period of weeks only by virtue
of their substantial carbon fixation rates.
The heterotrophic microbes from the algal habitat
removed much of the available labelled DOC from the incubation medium over the course of a few hours. If indeed
the DOC consists primarily of useful metabolic intermediates, the microbes might scavenge them from the
water by some active transport mechanism against a concentration gradient. Additionally, if the microbes were
previously adapted to the availability of such substrates in
their habitat, such transport would occur without a lag
time for the potential induction of necessary permeases.
The observation that the DOC removal rate increases
linearly with DOC availability over the range of concentrations measured suggests that such a presumed active
transport has not yet reached saturation. However, the
same result is also consistent with the possibility that DOC
removal is due to a passive process such as diffusion of
labile molecules into microbial cells, if the molecules are
quickly metabolized in some way to maintain the neces~
sary concentration gradient.
42
The populations o f Enteromorpha spp. which d o m i n a t e
the intertidal flats o f Coos Bay in s u m m e r a n d fall, and
which comprise a substantial part o f the eelgrass communities, contribute large quantities o f organic m a t t e r to
the estuary. Much o f this photosynthetically fixed material
enters the environment as D O C . All o f the typical estuarine fluctuations tested here increased D O C release. Most
o f this organic m a t t e r p r o b a b l y consists of labile metabolic
intermediates, which the heterotrophic microbes readily
utilize. This estuarine carbon p a t h w a y is characterized b y
short residence times in any o f the components; thus, such
a material a n d energy flux would p r e s u m a b l y be underestimated by static m e a s u r e m e n t s o f any single component.
Acknowledgements. This work was p e r f o r m e d as partial
fulfillment o f the degree o f Doctorate o f Philosophy at the
Oregon Institute o f M a r i n e Biology, University o f Oregon,
Eugene, Oregon, USA. This work was s u p p o r t e d by N I H
Training G r a n t 5T32 2 G M 07257 in Systems a n d Integrative Biology, and b y a G r a n t - i n - A i d o f Research from
Sigma Xi, the Scientific Research Society.
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Date of final manuscript acceptance: November 18, 1982.
Communicated by N. D. Holland, La Jolla