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PHOSPHORUS CYCLING IN AN EELGRASS
(ZOSTERA MARINA L.) ECOSYSTEM1
C. Peter McRoy, Robert J. Barsdate, and Mary Nebert
Institute
of Marine
Science,
University
of Alaska,
College
99701
ABSTRACI’
Rates of uptake and excretion of phosphorus by both roots and leaves of eelgrass (Zostefu
mwina L. ) were dependent on the orthophosphate
concentration
of the medium. In a typical
shallow tidal pool dominated by eelgrass, the interstitial
reactive phosphorus concentrations
of the sediments were as high as 75 pg-atom/liter,
while in the water they were ca. 2. The
plants absorbed 166 mg P/m2-day from the sediments, assimilated 104 in the production
of
fresh eelgrass, and excreted 62 into the water. An amount equivalent to about 41% of the
reactive phosphorus excreted, or 3 metric tons P/day, was exported from the lagoon into
the Bering Sea. These results add a new pathway to the phosphorus cycle for estuaries
containing vascular plants.
INTFLODUCTION
The cycle of phosphorus in shallow water
differs from the relatively simple one in
the open sea (e.g. see Harvey 1957) by the
interaction with bottom sediments. Studies
of estuaries by Rochford ( 1951)) Pomeroy
( 1960)) and Pomeroy et al. ( 1965, 1969)
indicate a dynamic interaction of the phosphorus in the water column with that in
the surface sediments. This interaction is
restricted to at most the upper few centimeters of sediment; below this phosphorus
is accumulated. Thus particulate phosphorus, in many environments largely from
organic detritus, is buried and lost from
short-term circulation. Recent studies have
revealed a further complication
to this
cycle in shallow waters : In areas containing
rooted aquatic plants phosphorus from the
deeper sediments can be returned to the
water via uptake by roots, incorporation into
the leaves, and release into the water.
For a time it was thought that phosphorus
was returned to the water column principally through detritus as portions of the
plant die and slough off (Pomeroy et al.
.I Financial support was provided to the University of Alaska from the Water Quality Office of
the Environmental
Protection Agency (Grant 18050
DKX), the US. Atomic Energy Commission (Contract AT 04-3-310 PA4), the National Science Foundation (Grant GB-8274),
and the Arctic Institute
of North America under contractual agreement with
the Office of Naval Research.
Contribution
146
from the Institute of Marine Science.
LIMNOLOGY
AND
OCEANOGRAPHY
1969). We now know that aquatic vascular
plants actively transport phosphorus from
the sediments and release it into the water
-a mechanism suggested by Foehrenbach
( 1969) and demonstrated experimentally
for a closed system by McRoy and Barsdatc
( 1970). In the latter study we determined
that phosphorus absorption by eelgrass
( Zostera marina L. ) is greatest in the light
and can occur in both leaves and roots, with
active transport to all parts of the plant
occurring rapidly after absorption.
Phosphate removed from solution by the roots
and rhizomes is returned in part to the
surrounding water through the leaves, suggcsting that rooted aquatic plants may act
either as a sink or source for dissolved phosphorus in the water. Reimo’ld found a similar mechanism in Spartina (L. R. Pomeroy’,
personal communication).
In this paper we document a mechanism
of phosphorus transfer from the sediment
to water via eelgrass and evaluate the importance of this pathway in the phosphorus
cycle of an ecosystem dominated by eel.grass. The studies were carried out i:n
Izcmbek Lagoon, an embayment of the
Bering Sea at the tip of the Alaska Peninsula
( Fig. 1). The lagoon contains vast eelgrass
meadows and has been the site of celgrass
community research since 1963 ( McRoy
1966, 1970a).
We arc grateful to R. D. Jones, Jr., fclr
use of the facilities of the Izcmbck Marinc
Station, WC also appreciate the assistance
58
JANUARY
1972,
V. 17( 1)
PHOSPHORUS
59
IN EELGRASS
forced out of the core sections through a
glass-fiber :filter ( Whatman GFC ) , 1 mg
Hg/liter was added as mercuric chloride,
and analyses were made for total dissolved
phosphorus (Menzel and Corwin 1965),
reactive phosphorus (Murphy
and Riley
1962)) and unreactive phosphorus ( presumably organic) by difference.
The water
content of the section was determined by
the ratio of wet weight to dry weight.
FIG. 1.
areas.
Map
of Izembek
Lagoon
and adjacent
of M. T. Gottschalk with field and laboratory
work and thank G. D. Sharma for providing
scdimcnt grain-size analyses and J. J. Goering for critically reading the manuscript.
METHODS
Phosphate uptake in eelgrass
Whole turions (a clump of leaves attached to a rhizome) or turions with leaves
and stems separated from the roots and
rhizomes were wiped free of epiphytes,
placed in bowls containing filtcrcd (0.45-p
membrane filter ) Izembck Lagoon water,
to which carrier-free 92P-NaI12P04 tracer
was added, and incubated under natural
light and temperature (range lo-12C). After
a 20-hr incubation the plants were removed
from solution, scctioncd to prevent migration of isotope, dried, weighed, pulverized,
and 32P activity was dctcrmincd with a G-M
gas flow detector. Two seawater solutions
were used, one containing 30 pg P/liter
(the natural level) and the other made up
to 2,000 ,ug P/liter with orthophosphate,
Phosphorus uptake was calculated from the
observed activity in the plant material and
initial specific activity of the solutions.
Interstitial
water chemistry
Cores 235 cm long and 7 cm in diamctcr
were scgmentcd at <5 cm intervals and
extracted with a minimum of contact to air
directly into a sediment-squeezing apparatus ( Recburgh 1967). Interstitial water was
Water chemistry
Both reactive and unreactive dissolved
phosphorus were analyzed in the water
column over the cclgrass beds as above. In
addition particulate phosphorus was determined on HA Milliporc
membrane filters
after persulfate digestion (modified from
Menzel and Corwin 1965). Supplcmcntary
studies using the same analytical techniques
wcrc carried out in waters of the Bering Sea
adjacent to Izembck Lagoon and in Glazenap Pass, one of the three channels bctwccn
Izembek and the Bering Sea.
Sediment size analysis
Particle size analysis of the sediment
cores was dctcrmined using standard sicvc
and pipette techniques (0.5 phi interval:
Krumbein and Pettijohn 1938).
RESULTS
Sediments and interstitial water
Sediment: cores were taken in a large tide
pool (about 100-m diam) containing a dense
cclgrass population and in a small tidal
drainage tributary, barren of eelgrass, less
than 50 m away. Both arcas were covcrcd
with about 30 cm of water at low tide, At
a core depth of 35 cm the composition and
grain size distribution in the sediments arc
nearly identical, but significantly
different
near the surface (Fig. 2). The sample from
outside the eclgrass bed grades from fine
sand at the surface to medium sand at a
depth of 35 cm and contains relatively
small amounts of silt, clay, and organic
matter. The core from the tidal pool showed
only silt-size and finer material at the surface, grading into a medium sand over a
20-cm span. The water content is rather
60
C. I?. McROY,
WATER CONTENT
0’
0
1.0
I
(g wet/g
2.0
R.
J.
BARSDATE,
dry)
3.0
4.0
5-
IO -
15 -
I
20-
ii
x
25 -
0
0
OUTSIDE
EELGRASS
0
IN
OF
BED
EELGRASS
BED
30
FIG. 2.
Water content in sediments as a function of sediment depth.
uniform in the channel core but varies
roughly in proportion to the abundance of
fine sediments in the tidal pool core. The
higher porosity of the tidal pool surface
sediments, indicated by the water content,
results from the abundance of fine-grained
matter deposited in the eelgrass stand.
Rates of sedimentation, particularly for silt,
clay, and organic detritus, are high in eelgrass beds ( Milne and Milne 1951).
In the tidal no01 the eelgrass rhizomes
propagate horiz&rtally almosF completely in
the laver of oxidized surface sediments,
while the roots extend into the reduced
sediments below. The abundance of roots
declines below a depth of 5 cm, few living
roots being found below 10 cm. The thickness of the oxidized zone in the celgrass
(1 cm) is the same as that observed by
Roysen Jensen (1914) in eelgrass beds off
Denmark. In the small scour channel the
oxidized zone extended to a depth of about
2 cm, and in both cores the deeper interstitial water contained dissolved sulfides in
concentrations of about 1 ppm.
AND
M.
NEBERT
Dissolved reactive phosphorus levels are
high in the upper 10 cm of the tidal pool
core fluids, with a maximum of 75 pg-atom,’
liter between 1 and 5 cm below the surface,
and decrease at greater depths to <lo. Out,side the cclgrass area reactive phosphorus
was much lower in the sediments, as in the
deeper portions of the tidal pool sediments
(Fig. 3). For dissolved unreactive phosphorus the situation is reversed, with somewhat higher levels in the channel core.
The root system of eelgrass is not exten
sive, so the zone from which it can absorb
nutrients is limited roughly to the upper
10 cm of reduced sediments. The reservoir
of reactive phosphorus available in the
interstitial water in this layer of the tidal
pool sediments is about 96 mg P/m2. An
additional amount exchangeable with dissolved forms and presumably available for
plant growth exists as particulate P in con
tact with the interstitial fluids. Only about
1.4% of the 32P injected into reduced Izem.bek Lagoon sediments rcmaincd in solution
after 24 hr, the remainder being taken up
by the particulate portion of the sediments.
If we assume that the 32P uptake is a mea-.
sure of the labile particulate phosphorus
(Olsen 1965) the total amount of phosphorus
available for plant growth is :
lOO/1.4 X 96 mg P/m2 = 6,900 mg P/m2.
This is about 70 times that present in the
interstitial water.
Exports from Ixembek Lagoon
Phosphorus concentrations in the water
flowing through Glazenap Pass on flooding
and ebbing tides reveal a net movement o:F
total dissolved reactive phosphorus out o:F
the lagoon. Samples taken over 14 tidal
cycles in June and July had :mean dissolved
reactive phosphorus concentrations of 0.77
pug-atom P/liter during flood tide and 1.06
during ebb; six tide cycles sampled in September showed mean levels of 1.39 pg-atom
P/liter at flood and 1.70 at ebb, and four
sets of samples in October showed 1.12 pgatom P/liter on the flood tide and 1.39 on
the ebb. Over the entire period the mean
net flow of reactive phosphorus was 0.29
pg-atom P/liter out of Izembek Lagoon into
PHOSPHORUS
Reactive
40
Unreactive
OUTSIDE OF
EELGRASS BED
0
IN EELGRASS
BED
concentrations
in interstitial
the Bering Sea (Table 1). Relatively low
concentrations of dissolved unreactive and
particulate
phosphorus moved into the
lagoon through Glazer-rap Pass during June,
July, and September, but the net total phosphorus flow was always seaward. Large
quantities of eelgrass leaves were transported out of the lagoon in suspension,
TABLE
1.
P (pg-atom/liter)
60
0
Phosphorus
61
EELGRASS
P (pg-atom/liter)
20
FIG. 3.
IN
water
as a function
0
OUTSIDE OF
EELGRASS BED
0
IN EELGRASS
BED
of sediment
particularly during September and October.
This material, which often floated in long
windrows, ‘was excluded from the analyses
as our sample volumes were too small to
provide a useful measure of its abundance.
We estimated the surface area of Izembek
Lagoon to be 218 km2, the mean tide height
0.98 m, and the tidal prism to include a
Glamnap Pass phosphorus flow, 1969. Concentrations are in ,qatom
June and July
Mean
cliff
Net
direction
Reactive dissolved
Unreactive
dissolved
Particulate
0.29
0.06
0.00
out
Total
0.23
depth.
P/liter
September
Md?F
1
October
Net
direction
c&n
Net
direction
out
In
In
0.27
0.24
out
out
fi
0.31
0.09
0.14
0.21
Out
Out
0.08
Out
0.72
Out
62
C. P. McROY,
R.
J.
BARSDATE,
AND
M.
NEBERT
162'30'
FIG. 4. Dissolved reactive phosphorus distribution
in the Bering Sea adjacent to Izembek
1968 (RV Acona cruise 066). Concentrations
in pg-atom P/liter.
volume of 1.7 X IO* m3, resulting in a 68%
exchange of the 2.5 x 10s I113 present at
mean high tide. Assuming the net outflow
of dissolved reactive phosphorus at Glazenap Pass, 0.29 pug-atom P/liter, to be the
same at the other passes, then 1.47 x lo3
kg P is exported from the lagoon as reactive
phosphorus during each tidal cycle.
A lobe of relatively high surface concentrations of dissolved reactive phosphorus
extends out into the Bering Sea from the
passes between the lagoon barrier islands
(Fig. 4). In June the water of highest
phosphorus levels is located off Glazenap
Pass at the southwest end of the lagoon.
That this phosphorus plume originates in
Izembek is suggested both by its proximity
to the lagoon and by the fact that phosphorus concentrations inside the lagoon are
more than twice as high as those in the
Bering Sea. The phosphorus plume is presumably displaced to the west of the lagoon
by tidal currents having a strong southwcstcrly flow on the ebb tide (Hebard
1961) .
During a Scptcmber 1970 cruise (RV
Lagoon,
June
ACOM 103) dissolved reactive phosphorus
values in the range of 0.59-0.78 pug-atom P/
liter occurred roughly within the area enclosed by the 0.40 isopleth in Fig. 4. During
the same period surface reactive phosphorus
varied between 0.26 and 0.54 pg-atom/liter
at stations farther north along 164” W in
the Bering Sea.
Diel variations in the lagoon
In June and September we measured
total, particulate, and reactive and unreactive dissolved phosphorus in the eelgrass
beds of a shallow (ca. 30 cm, low tide; 100
cm, high tide) tide pool in Izembek Lagoon.
Concentrations
varied markedly in both
sampling periods, with maxima during ebb
tides ( Figs, 5 and 6). In June the increases
were associated with both particulate and
dissolved reactive phosphorus but in Scptcmbcr were restricted to :reactive phosphorus. Reactive phosphorus concentrations
in June went from a range of 0.7-1.7 FE;atom P/liter to peaks in a range from 3.54.8, and in September from a mean of 2.0
at high tide to 5.0 at low tide.
PHOSPHORUS
Time
17 June 1969
FIG. 5.
FIG. 6.
IN
63
EELGRASS
19 June
18 June 1969
Diel phosphorus
Diel phosphorus
concentrations
concentrations
in Izembek
in Izembck
Lagoon,
Lagoon,
June.
September.
1969
64
C. I?. McROY,
BARSDATE,
by eelgrass from
and high (2,000
pg Pod-P/liter)
phosphorus concentration.
Incubations were for 20 hr under natural conditions of
light and temperature;
single experiments
TABLE
2.
R. J.
Uptake of “P-phosphate
seawaterof low (30 ,ug PO,-P/liter)
Phosphate uptake
( /.a P/g plant )
Whole plant, leaves
Whole plant, roots and rhizomes
Detached leaves
Detached roots and rhizomes
Low
High
11
22
9
12
320
280
520
500
Standing stock
The avcragc midseason standing stock of
eelgrass is 1,040 g dry wt/m2 in the tide
pools with 68% dry weight in leaves and
stems and 32% in roots and rhizomes (McRoy 1970b). The eelgrass contained from
3.4-7.0 mg P/g dry plant, with a mean of
5.0 mg/g in roots and rhizomes and also in
leaves, somewhat higher than published concentrations ( 1.6 mg/g: Vinogradov 1953;
3.9 mg/g: Burkholder and Doheny 1968).
On an arcal basis this indicates a pool of
phosphorus in the eelgrass of 3,560 mg/m2
in the leaves and 1,650 in the roots and
rhizomes, or a total of 5,210 mg/m2, of the
same magnitude as our estimate of the
available phosphorus reservoir in the sediments (see above). The average concentration of reactive phosphorus is about 30 pg
P/liter in the water, resulting in a pool of
930 mg P/m2 in the water column, depending on the stage of the tide and of the
sharp peaks in concentration noted above.
Dissolved unreactive and particulate phosphorus in combination make up an additional 6-20 mg P/m2.
Uptake of 82P-labeled phosphate
Rate of uptake by whole and bisected
eelgrass in vitro was determined for two
concentrations of phosphate, one (30 pg or
0.97 PI;-atom dissolved reactive phosphorus/
liter) close to the mean concentration in
the water of Izembek Lagoon and the other
(2,000 pg or 65 pug-atom Pod-P/liter) within
the range of sediment interstitial water.
Phosphate was taken up by leaves and
roots and rhizomes whether detached from
the plant or not ( Table 2). The rate of
AND
M.
NEBERT
uptake for attached leaves and stems in
high phosphorus concentration was 29 times
that in low phosphorus concentrations; the
detached leaf rate was 58 times higher. For
roots and rhizomes the rate was 12.7 times
higher in the high phosphorus concentration
when intact and when detached it was 42
times higher. Although the proportional
uptake rate (plant
phosphorus
uptake
divided by water phosphorus concentration) is somewhat less at the high phosphate
level, the rate of phosphorus uptake evidently depends on the concentration
of
available phosphorus in the medium.
DISCUSSION
Previously we reported that eelgrass was
capable of transporting POa both from the
sediments to the water column and the
reverse (McRoy and Barsdate 1970). Transport rates were calculated for a closed
partition system where similar PO4 concentrations (25 pg P/liter)
existed in water
surrounding roots and leaves, Phosphorus
flux data from a set of these early experimcnts (for eelgrass in artificial light at 15C
for 50 hr), originally reported per plant,
are presented here (Fig. 7, left) per gram
dry weight of plant. The 50 hr 32P uptake
experiments seriously underestimated
the
actual flux rates of phosphorus in eelgrass
because of the limited volume of the experimental container and the resultant changes
in 32P specific activity with time. Therefore,
somewhat arbitrarily, we have taken these
rates to be an adequate representation of
the daily flux of phosphorus, compensating
in part for their underestimation.
Eelgrass in Izcmbek Lagoon grows with
its roots in sediment containing a high concentration of dissolved phosphate in the
interstitial water and the leaves in water
with a relatively low PO4 concentration.
The factor of 12.7, representing the increase
in the rate of phosphorus accumulation by
the roots of whole plants in 2,000 pg P/liter
over that in 30 pg P/liter solutions, has been
applied to the plants’ phosphorus pathways
originating in the roots ( Fig. 7, right). This
we consider to be a reasonable approximation of nature. Converting the phosphorus
transports per gram plant-day (Fig. 7, right)
PHOSPHORUS
IN
65
EELGRASS
SEAWATER
SEAWATER
(25flg
P/liter)
(25 pg P/liter)
t
I
-7.22
LEAVES
t
-122
LEAVES
I 1
I 1
.
18.80-
1.48--t
8.20
0.74
(25Ng
I
I
8i!50
1.39
104. I4
0.74
INTERSTITIAL!
WATER
INTERSTITIALv
WATER
P/liter)
.
I
(2000
yg PI liter)
L-
FIG.
7. Calculated daily phosphorus flux through 1 g dry wt of eelgrass. Left: Uniform dissolved
reactive phosphorus concentration
in water. Right : Phosphate gradient similar to the natural environment. Units are pug P/g plant-day.
to surface area basis results in a net flow
of 62.4 mg P/m2-day from the eelgrass into
the surrounding water ( Fig. 8).
The observation of Boyd (1969) that
some aquatic vascular plants gain a competitive advantage over phytoplankton
by
absorbing and storing phosphorus before
the period of maximum growth is not supported by the dynamic phosphorus cycle we
have observed and measured in eelgrass.
Our data indicate that the standing concentration of phosphorus in the tissues would
not maintain the plants for an extended
period, so that resupply from external
sources is a continuing necessity.
The net transport rate of phosphorus from
eelgrass plants into the water can be used
to estimate changes in concentration in the
water over eelgrass beds. At the site of
the diurnal studies described above, with a
water depth of 30 cm at low tide lasting for
about 6 hr, the eelgrass could pump 15.6 mg
P/m2 to the water, resulting in an increase
of 1.6 pug-atom P/liter during the period.
This is an underestimation due to the advectivc contributions of phosphorus from plants
66
C. P. McROY,
R.
J.
BARSDATE,
SEAWATER
62.4
I
-27.
I-
I
89.5
ROOTS
81
RHIZOMES
(1650)
(1650)
-18.0 -18.0
(96)
FIG. 8. Net daily movement
phosphorus
(mg/
m2) in an eclgrass stand. Amount of phosphorus
( mg/m2) in each compartment
is in parentheses.
located near the margins of the pools in
less than 30 cm of water. Comparisons with
the observed data ( Figs, 5 and 6)) which
show reactive phosphorus peak amplitudes
of about 3 pug-atom P/liter ( 28 mg P/m2)
during about 4 hr, suggest that this mechanism is adequate to account for the periodicity in reactive phosphorus in these beds.
Pomeroy et al. (1969) pointed out that
Spartina in a salt marsh utilized phosphorus
through the sediments and that this eventually would be returned to the sediments
In Izcmbck
as particulate
phosphorus.
AND
M.
NEBERT
Lagoon, eclgrass is the dominant primary
producer-quantitatively
far more important than the remainder of the benthic
components or planktonic algae-and
here
the amount of particulate p’hosphorus produced by eelgrass and potentially available
for herbivores or entry to the detritus cycle
reaches an impressive magnitude.
McRoy (1970b) estimated the net daily
productivity
of eelgrass to be about 2% o.E
the standing stock. Using our estimate o:E
standing stock of phosphorus (5,210 mg
P/m2) we calculate the daily increment o.F
phosphorus involved in the production of
fresh eelgrass to be 104.2 mg P/m2-day. The
calculated rate of phosphorus uptake by
eelgrass synthesized from i,n vitro experiments is the sum of the fluxes to leaves and
roots plus rhizomes in Fig. 8 (45.1 mg/m2 day). For the eelgrass beds of the entire
lagoon rather than the tide pool, the rates
would be 15% higher, due to the slightly
greater mean standing stock in the lagoon
( 1,200 g/m2 vs. 1,040 in the tide pool). A
portion of this phosphorus is cycled locally
within the lagoon, but the export of floating
eelgrass provides a presently unmeasured
but no doubt substantial contribution
o.F
phosphorus to the open sea and to its benthic communities.
The amounts of phosphorus projected
here as leaving the sediments, well ove:r
100 mg P/m2-day for nearly 6 months of
the year ( May-October),
must be balanced
by resupply, as the total labile phosphorrrj
in the eelgrass root zone of the sediments
is only about 7,000 mg/m2 (interstitial and
labile). Sedimentation of detritus is rapid
in the eelgrass beds; this presumably results
in rather intense local recycling of phosphorus. However, the substantial flux of
phosphorus out of the lagoon strongly suggests the presence of other phosphorus inputs, Rain and stream flow provide only a
small portion of the water exchanged in
the lagoon, as the salinity difference between inflow and outflow in the passes is
less than 1%0( McRoy 1966), making it unlikely that significant amounts of dissolved
phosphorus are brought in by freshwater.
The Bering Sea could become a source for
phosphorus input into the lagoon during
PHOSPHOIKJS
winter, However, circumstances involving
both the reversal of the summer phosphorus
concentration gradients and the deposition
of phosphorus in lagoon sediments seem
unlikely.
Black volcanic sands, such as make up
the bulk of the sediments of the lagoon,
usually are relatively rich in phosphorus and
also undergo chemical weathering rather
rapidly in comparison with sands derived
from most other igneous rock types. We
suspect that chemical alteration of the inorganic sediments supplies an important
flux of labile phosphorus within the lagoon.
The export of dissolved reactive phosphorus from the lagoon prdvides a contribution to the sea of 1.47 X lo3 kg P/tidal cycle
or about 3 x 10” kg P/day. If the assumption is made that this originates in the 116
km2 of eelgrass beds covering roughly 50%
of the lagoon, the reactive phosphorus flux
from the eelgrass beds is 25.86 mg P/m2day. Our estimate of the reactive phosphorus translocation rate from sediments to
water via the plants is 62.4 mg P/m2-day.
This flux is high enough to sustain the
observed phosphorus flow from the lagoon
and, in addition, provides an explanation for
the consistantly high phosphorus concentrations found in the lagoon. This pathway,
the pumping of reactive phosphorus from
sediment to water by aquatic vascular
plants, adds a new and quantitatively
important phosphorus pathway to estuarine
systems and is likely to function in a similar
manner in tidewater and freshwater systems,
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