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Seagrass productivity: Carbon uptake experiments in eelgrass, Zostera marina
Aquaculture, 4(1974)131-137 o Elseviear Scientific Publishing
Company,
SEAGFCASS PRODUCTIVITY: GRASS, ZOSTERA MARINA C. PETER Institute
Amsterdam
-
Printed
in The Netherlands
CARBON UPTAKE EXPERIMENTS IN EEL-
McROY of Marine
Contribution (Received
Science,
No. 216,
University
Institute
of Alaska,
of Marine Science,
Fairbanks,
Alaska
University
(U.S.A.)
of Alaska,
Fairbanks
May 13, 1974)
ABSTRACT McRoy, C.P., 1974. Seagrass productivity: marirma. Aquaculture, 4: 131-137.
carbon
uptake
experiments
in eelgrass,
Zostera
The productivity of eelgrass, Zostera marina L., was measured in relation to light and season using 14C. Net productivity during the summer averaged 56 pg C/g dry weight per langley and on an area1 basis 4.8 g C/m* per day. The total production during the growing season a’as calculated to be 812 g C/m* with at least a twofold turnover of the standing stock during this period. The c.ptake of carbon in relation to light intensity is hyperbolic below 50% light followed by some inhibition at higher intensities. This response is described using MichaelisMenton kinetic equations. These experiments indicate that light saturation occurs at very low intensity. The half-saturation constant (KL~) was 12.5% of surface light.
INTROWJCTION
Seagrass meadows are highly productive ecosystems. The primary production of these systems is to a great extent due to the productivity of the seagrasses although benthic epiphytes and planktonic algae are certainly contributors. Although numerous reports of productivity measurements of seagras:;es exist (reviewed by McRoy and McMillan, in press) only a few studies examine the detail of the productivity mechanism. Most data are based on short term changes in standing stock (a minimum estimate of net production) and only two have used readioact,ve carbon (Brylinski, 1971; Dillon, 1971). In this study the productivity of eelgrass, Zostera marina L., in relation to light intensity was measured using 14C. The measurements were made in Izembek Lagoon, an embayment of the Bering Sea that contains one of the most e:&ensive eelgrass meadows in Alaska (McRoy, 1970). In this lagoon the eelgrass meadows occupy the shallow waters of the upper sublittoral; because of the tidal periodicity a large portion of the leaves float on the surface during daylight hours that coincide with low tides. The long days of high latitudes and the shallow waters of the lagoon provide optimal conditions for photosynthes#is and the lagoon truly abounds with dense stands of eelgrass..
132
METHODS
Carbon uptake, an estimate of net productivity, was measured with “C using techniques developed for fresh-water macrophytes (Vollenweider, 1969). Eelgrass plants, including roots, were collected from Izembek Lagoon shortly before incubation, cleaned of sediment and epiphytes, and placed in filtered sea water in glass bottles. An experiment consisted of pairs of bottles, covered or not, with neutral density filters resulting in five light intensity levels (0, 10, 25, 50 and 100% of surface light) and incubated for 4 h in the lagoon in about 20 cm of water. Water temperatures and solar radiation were measured during each experiment as were the pH and salinity of the filtered sea water. The isotope was added as H14COT. At the end of an experiment the plants were rinsed, bottled and frozen in the dark. Further processing of the plants involved drying in a desiccating oven, fuming with HCl, cornbusting weighed samples and trapping the CO2 in scintillation solution, and finally measuring radioactivity with a liquid scintillation counter. Samples of leaves and roots were counted separately. All counts were corrected for dark uptake, background and quenching. Experiments were done every other week from late June to August and once again in October. Biomass samples for the measurements of eelgrass standing stock were also collected biweekly, using a quantitative sampler described by Grtintved (1958) and the procedures outlined by McRoy (1966). RESULTS
Carbon uptake in relation to light by eelgrass was measured on nine occasions from the end of June to August and once again in October (Fig.1). This figure summarizes the results of duplicate observations of the 100% light experiments, i.e. the natural light conditions. The results of the 4-h experiments were converted to daily values by multiplying the rate per langley by the total langleys available during the day which assumes that the 4-h experiments are representative of the daily rate. The trend and seasonal maximum shown by the curve is then a result of the increasing light and temperature conditions during the summer as well as the increasing biomass of leaves. The average net productivity per gram for the 100% experiments was 56 yg C/g dry weight per langley with a range of 8-133 pugC/g dry weight per langley (Table I). On a unit area basis the average net productivity was 4.8 g C/m2 per day and ranged from 0.8 to 13 g C/m* per day. From the mean net productivity (56 pg C/g dry weight per langley) the total production during the summer growing season (June to August) can be calculated. The total light for the period was 27 028 langleys and the leaf biomass (g dry weight/m2) for each month (Fig.2) was 203 for June, 753 for July, and 741 for August. These data provide an estimated net production for the period of 812 g C/m* and a turnover of the standing stock of at least twice during this period.
133
&,;‘,s JUfE
r;"',~1;'~';,I;';',;Is';,;,i J:"y
dug
Fig.1. The seasonal means (3f duplicate
~~~
B 1
IO00
M Q F -Q Q
At Lagoon.
by eelgrass in Izembek surface light intensity.
Data
are
4
Q
2 PI k_
Sl$
course of carbon uptake measurements for 100%
/-------.---_____,
Boo-
fioo-
200
0
,A
c 115
--
/
4on-
/
---
lo
1 ’ ’ I5 20 25 JWW
’
’ 5
’
I
’
1’
’
I@ 15 ;r, 25 Ju&
--------v
‘4’ ’
i ’
5
1 I5’ a ’ ’ 25
c
AlJQUSi
Fig.2. T’he seasonal course of eelgrass standing of ten replicate measurements at each time.
stock
’
’
5
I
I
’
1
Ii’ I5 20 25 September
in Izembek
’
’ IO/ I5i 201 25I
5
1
fk‘ober
Lagoon.
Data are means
of carbon
10
25
50
100
?? S.D. Range
x S.D. Range
x S.D. Range
(%I
Light intensity
I
x S.D. Range
Summary
TABLE
33
31
32
32
on eelgrass. Data are averages
931 459 298-l 709
1 182 450 355-l 705
929 484 286-l 787
504 389 116-l 182
56 43 8-133
130 73 17-255
184 96 29-336
216 80 71-328
Carbon uptake ~mg C/g per h mg C/g per langley
experiments
Number of observations
uptake
11 8 5-30
27 11 11-51
42 25 19-93
42 17 20-67
mg C/g per day
5 4 l-13
11 6 3-21
17 13 5-40
19 15 3-54
per day
October
g C/m’
from all dates except
17 15 l-40
20 13 6-41
15 11 5-34
20 20 4-58
per g
% carbon
34 23 5-70
38 18 17-65
31 17 10-57
37 19 15-70
per m2
transfer
to roots
135
In all experiments regardless of light intensity a portion of the carbon fixed by the leaves was translocated to the roots and rhizomes. This portion averaged 17% of the total carbon fixed on gram dry weight basis and 34% on an area1 basis. The results of the light experiments indicate a hyperbolic, light-limited response for the portion of the curve up to 50% light followed by inhibition at higher intensities (Fig.3). The first portion of the curve can be quantitatively described in kinetic parameters by the Michaelis-Menton equations, a technique recently applied to phytoplankton productivity and nutrient uptake (MacIsaac and Dugdale, 1972). The maximum rate of carbon uptake (V,,,) is 1.18 rag C/dry weight per h, and the light half-saturation constant (KLt) is 12.5%. The latter constant designates the light intensity for one-half the maximum rate of carbon uptake. The’se kinetic parameters can then be used in the Michaelis-Menton kinetic equation to calculate the carbon uptake rate for in situ conditions once the light intensity has been measured. The relationship is:
where V = carbon uptake rate in mg C/g dry weight per h, V,, = maximum uptakla rate (= 1.18 mg C/g dry weight per h), S = in situ light intensity as % of surface intensity, KLt = light intensity where V = V,,,/Z = 12.5%.
Surface
Light Intensity /Langleys /hri
6 I
f2 1
Ql
24 I
Vmox = I I8 mgC/g-dry-hr KI_+ = 12.5 %
3 9 CO5 -0” k c,
I8 I
/
P 0
/’
,
0
20
,
I 40
Surface
, 60
I
, 80
I
J
fOC
i /ght lntenslty f%)
Fig.3. Carbon uptake in eelgrass in relation to surface light intensity. Kinetic parameters of maximum uptake rate (I’,,) and light intensity (KL~) at one-half V,, are indicated. Data are mean uptake rates from all experiments done through the summer and mean light intensi.ties for the experiments.
This equation should only be used as an approximation of the actual produc ivity since a considerable variance exists in these measurements (Table I). Also it will overestimate the actual rate for light intensities over 50%. This inhibition at high light intensities could be the direct effect of intense light on the photosynthetic process or it could be involved with nutrient supply or some combination of these factors. These results indicate that photosynthesis in eelgrass is probably only rarely light limited and that light saturation occurs at low light intensities. In these experiments the average light intensity at one-half V,,, (the 12.5% level) corresponded to 0.052 langleys/min. DISCUSSION
The measurement of the productivity of seagrasses is subject to several as yet quantitatively undefined errors. A large portion of the volume of a leaf consist of lacunae, large gas-filled tubes, and it is likely that some of the products of photosynthesis are internally recycled and not measured. This has been demonstrated for some submerged fresh-water vascular plants (Hartman and Brown, 1967). In addition some carbon fixed by photosynthesis is undoubtably lost by secretion of soluble organic compounds. Brylinski (1971) examined several seagrass species in Florida and found this loss to be about 2% of the total carbon fixed. Extrapolation of the magnitude of loss from the subtropical species to eelgrass in Izembek Lagoon is at the least reasonable. Carbon is also lost in respiration, which is usually assumed to be the same in the light as in the dark, but increasing evidence suggests that respiration may be reduced in the light and that efficient refixation of respired CO2 occurs in submerged plants in the light (Wetzel and Hough, 1973). On the other hand, Hough (R.A. Hough, personal communication) has found some evidence for photorespiration in the seagrasses Cymodocea sp. and Halophila ovalis. The result of this process is an increased loss of CO2 in the light and an effective reduction in the efficiency of photosynthesis. In spite of the possible errors described above the productivity of eelgrass is very high compared to other marine primary producers. It is probable that the total annual production is on the order of 1000-l 500 g C/m’, a quantity more than five times that of the phytoplankton in the North Pacific (KoblentsMishke, 1965). The productivity rates measured in this study compare closely with those fron other studies using other techniques. In a recent review of productivity data If seagrasses, McRoy and McMillan (in press) considered 4 g C/m’ per day an average rate for tropical as well as temperate species. The average rate from the present study is 4.8 g C/m2 per day, a surprisingly comparable rate, that once again confirms the view of seagrasses as one of the most productive ecosystems in the sea.
137
The kinetic analysis of carbon uptake as a function of light yields a quantitative expression that can be used to estimate eelgrass productivity under any conditions from ambient light measurements. The kinetic constants, however, are associated with considerable variability and need further documentation for eelgrass as well as other species. The light half-saturation constant (KLt) measured for eelgrass is very close to those observed for nitrogen uptake by phytoplankton in eutrophic waters (MacIsaac and Dugda.le, 1972) and this coincidence suggests a functional relationship for photosynthetic marine organisms. ACKNOWLEDGEMENTS
The technical assistance in field and laboratory of Tom Leue and Sally Dunker were invaluable to this study. The research is a part of studies of seagrass ecosystems supported by the Oceanography Section (Grant GA 30980) and the office of the International Decade of Ocean Exploration (Grant GX 37852) of the National Science Foundation. REFE:RENCES Brylinski,
M., 1971.
Release
of Dissolved
Organic
Matter
by Marine
Macrophytes.
Disserta-
tion, Dept of Zoology, Univ. of Georgia, Athens, 90 pp. Dillon, C.R., 1971. A Comparative Study of The Primary Productivity of Estuarine Phytoplankton and Macrobenthic Plants. Dissertation, Dept Botany, Univ. North Carolina, Chapel Hill, N.C., 112 pp. GrQntved, J., 1958. Underwater macrovegetation in shallow coastal waters. J. Cons. Int. Exp. Mer., 24( 1): 32-42. Hartman, R.T. and Brown, D.L., 1967. Changes in composition of the internal atmosphere of submerged vascular hydrophytes in relation to photosynthesis. Ecology, 48(2): 252-258. Koblents-Mishke, O.I., 1965. Primary production in the Pacific. Oceanology, 5(2): 104-116 Machaac, J.J. and Dugdale, R.C., 1972. Interactions of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Res., 19: 209-232. McRoy, C.P., 1966. Standing Stock and Ecology of Eelgrass (Zostera marina L.) in Izembek Lagoon, Alaska. Thesis, Univ. Washington, Wash., 138 pp.
McRc,y, C.P., 1970.
Standing stocks and related features of eelgrass populations in Alaska. J. Fish Res. Bd Canada. McRoy, C.P. and McMillan, C., in press. Productivity and physiological ecology of seagrasses. In: C.P. McRoy and C. Helfferich (editors), Seagrass Ecosystems: A Scientific Perspective, M. Dekker Inc., New York, N.Y. Vollenweider, R.A. (Editor), 1969. IBP Handbook. A Manual on Methods for Measuring Primary Production in Aquatic .Environments. 224 pp. Wetzel, R.G. and Hough, R.A., 1973. Productivity and role of aquatic macrophytes in lakes: an assessment. Pol. Arch. Hydrobiol., 20(l): 9-19.
Company,
SEAGFCASS PRODUCTIVITY: GRASS, ZOSTERA MARINA C. PETER Institute
Amsterdam
-
Printed
in The Netherlands
CARBON UPTAKE EXPERIMENTS IN EEL-
McROY of Marine
Contribution (Received
Science,
No. 216,
University
Institute
of Alaska,
of Marine Science,
Fairbanks,
Alaska
University
(U.S.A.)
of Alaska,
Fairbanks
May 13, 1974)
ABSTRACT McRoy, C.P., 1974. Seagrass productivity: marirma. Aquaculture, 4: 131-137.
carbon
uptake
experiments
in eelgrass,
Zostera
The productivity of eelgrass, Zostera marina L., was measured in relation to light and season using 14C. Net productivity during the summer averaged 56 pg C/g dry weight per langley and on an area1 basis 4.8 g C/m* per day. The total production during the growing season a’as calculated to be 812 g C/m* with at least a twofold turnover of the standing stock during this period. The c.ptake of carbon in relation to light intensity is hyperbolic below 50% light followed by some inhibition at higher intensities. This response is described using MichaelisMenton kinetic equations. These experiments indicate that light saturation occurs at very low intensity. The half-saturation constant (KL~) was 12.5% of surface light.
INTROWJCTION
Seagrass meadows are highly productive ecosystems. The primary production of these systems is to a great extent due to the productivity of the seagrasses although benthic epiphytes and planktonic algae are certainly contributors. Although numerous reports of productivity measurements of seagras:;es exist (reviewed by McRoy and McMillan, in press) only a few studies examine the detail of the productivity mechanism. Most data are based on short term changes in standing stock (a minimum estimate of net production) and only two have used readioact,ve carbon (Brylinski, 1971; Dillon, 1971). In this study the productivity of eelgrass, Zostera marina L., in relation to light intensity was measured using 14C. The measurements were made in Izembek Lagoon, an embayment of the Bering Sea that contains one of the most e:&ensive eelgrass meadows in Alaska (McRoy, 1970). In this lagoon the eelgrass meadows occupy the shallow waters of the upper sublittoral; because of the tidal periodicity a large portion of the leaves float on the surface during daylight hours that coincide with low tides. The long days of high latitudes and the shallow waters of the lagoon provide optimal conditions for photosynthes#is and the lagoon truly abounds with dense stands of eelgrass..
132
METHODS
Carbon uptake, an estimate of net productivity, was measured with “C using techniques developed for fresh-water macrophytes (Vollenweider, 1969). Eelgrass plants, including roots, were collected from Izembek Lagoon shortly before incubation, cleaned of sediment and epiphytes, and placed in filtered sea water in glass bottles. An experiment consisted of pairs of bottles, covered or not, with neutral density filters resulting in five light intensity levels (0, 10, 25, 50 and 100% of surface light) and incubated for 4 h in the lagoon in about 20 cm of water. Water temperatures and solar radiation were measured during each experiment as were the pH and salinity of the filtered sea water. The isotope was added as H14COT. At the end of an experiment the plants were rinsed, bottled and frozen in the dark. Further processing of the plants involved drying in a desiccating oven, fuming with HCl, cornbusting weighed samples and trapping the CO2 in scintillation solution, and finally measuring radioactivity with a liquid scintillation counter. Samples of leaves and roots were counted separately. All counts were corrected for dark uptake, background and quenching. Experiments were done every other week from late June to August and once again in October. Biomass samples for the measurements of eelgrass standing stock were also collected biweekly, using a quantitative sampler described by Grtintved (1958) and the procedures outlined by McRoy (1966). RESULTS
Carbon uptake in relation to light by eelgrass was measured on nine occasions from the end of June to August and once again in October (Fig.1). This figure summarizes the results of duplicate observations of the 100% light experiments, i.e. the natural light conditions. The results of the 4-h experiments were converted to daily values by multiplying the rate per langley by the total langleys available during the day which assumes that the 4-h experiments are representative of the daily rate. The trend and seasonal maximum shown by the curve is then a result of the increasing light and temperature conditions during the summer as well as the increasing biomass of leaves. The average net productivity per gram for the 100% experiments was 56 yg C/g dry weight per langley with a range of 8-133 pugC/g dry weight per langley (Table I). On a unit area basis the average net productivity was 4.8 g C/m2 per day and ranged from 0.8 to 13 g C/m* per day. From the mean net productivity (56 pg C/g dry weight per langley) the total production during the summer growing season (June to August) can be calculated. The total light for the period was 27 028 langleys and the leaf biomass (g dry weight/m2) for each month (Fig.2) was 203 for June, 753 for July, and 741 for August. These data provide an estimated net production for the period of 812 g C/m* and a turnover of the standing stock of at least twice during this period.
133
&,;‘,s JUfE
r;"',~1;'~';,I;';',;Is';,;,i J:"y
dug
Fig.1. The seasonal means (3f duplicate
~~~
B 1
IO00
M Q F -Q Q
At Lagoon.
by eelgrass in Izembek surface light intensity.
Data
are
4
Q
2 PI k_
Sl$
course of carbon uptake measurements for 100%
/-------.---_____,
Boo-
fioo-
200
0
,A
c 115
--
/
4on-
/
---
lo
1 ’ ’ I5 20 25 JWW
’
’ 5
’
I
’
1’
’
I@ 15 ;r, 25 Ju&
--------v
‘4’ ’
i ’
5
1 I5’ a ’ ’ 25
c
AlJQUSi
Fig.2. T’he seasonal course of eelgrass standing of ten replicate measurements at each time.
stock
’
’
5
I
I
’
1
Ii’ I5 20 25 September
in Izembek
’
’ IO/ I5i 201 25I
5
1
fk‘ober
Lagoon.
Data are means
of carbon
10
25
50
100
?? S.D. Range
x S.D. Range
x S.D. Range
(%I
Light intensity
I
x S.D. Range
Summary
TABLE
33
31
32
32
on eelgrass. Data are averages
931 459 298-l 709
1 182 450 355-l 705
929 484 286-l 787
504 389 116-l 182
56 43 8-133
130 73 17-255
184 96 29-336
216 80 71-328
Carbon uptake ~mg C/g per h mg C/g per langley
experiments
Number of observations
uptake
11 8 5-30
27 11 11-51
42 25 19-93
42 17 20-67
mg C/g per day
5 4 l-13
11 6 3-21
17 13 5-40
19 15 3-54
per day
October
g C/m’
from all dates except
17 15 l-40
20 13 6-41
15 11 5-34
20 20 4-58
per g
% carbon
34 23 5-70
38 18 17-65
31 17 10-57
37 19 15-70
per m2
transfer
to roots
135
In all experiments regardless of light intensity a portion of the carbon fixed by the leaves was translocated to the roots and rhizomes. This portion averaged 17% of the total carbon fixed on gram dry weight basis and 34% on an area1 basis. The results of the light experiments indicate a hyperbolic, light-limited response for the portion of the curve up to 50% light followed by inhibition at higher intensities (Fig.3). The first portion of the curve can be quantitatively described in kinetic parameters by the Michaelis-Menton equations, a technique recently applied to phytoplankton productivity and nutrient uptake (MacIsaac and Dugdale, 1972). The maximum rate of carbon uptake (V,,,) is 1.18 rag C/dry weight per h, and the light half-saturation constant (KLt) is 12.5%. The latter constant designates the light intensity for one-half the maximum rate of carbon uptake. The’se kinetic parameters can then be used in the Michaelis-Menton kinetic equation to calculate the carbon uptake rate for in situ conditions once the light intensity has been measured. The relationship is:
where V = carbon uptake rate in mg C/g dry weight per h, V,, = maximum uptakla rate (= 1.18 mg C/g dry weight per h), S = in situ light intensity as % of surface intensity, KLt = light intensity where V = V,,,/Z = 12.5%.
Surface
Light Intensity /Langleys /hri
6 I
f2 1
Ql
24 I
Vmox = I I8 mgC/g-dry-hr KI_+ = 12.5 %
3 9 CO5 -0” k c,
I8 I
/
P 0
/’
,
0
20
,
I 40
Surface
, 60
I
, 80
I
J
fOC
i /ght lntenslty f%)
Fig.3. Carbon uptake in eelgrass in relation to surface light intensity. Kinetic parameters of maximum uptake rate (I’,,) and light intensity (KL~) at one-half V,, are indicated. Data are mean uptake rates from all experiments done through the summer and mean light intensi.ties for the experiments.
This equation should only be used as an approximation of the actual produc ivity since a considerable variance exists in these measurements (Table I). Also it will overestimate the actual rate for light intensities over 50%. This inhibition at high light intensities could be the direct effect of intense light on the photosynthetic process or it could be involved with nutrient supply or some combination of these factors. These results indicate that photosynthesis in eelgrass is probably only rarely light limited and that light saturation occurs at low light intensities. In these experiments the average light intensity at one-half V,,, (the 12.5% level) corresponded to 0.052 langleys/min. DISCUSSION
The measurement of the productivity of seagrasses is subject to several as yet quantitatively undefined errors. A large portion of the volume of a leaf consist of lacunae, large gas-filled tubes, and it is likely that some of the products of photosynthesis are internally recycled and not measured. This has been demonstrated for some submerged fresh-water vascular plants (Hartman and Brown, 1967). In addition some carbon fixed by photosynthesis is undoubtably lost by secretion of soluble organic compounds. Brylinski (1971) examined several seagrass species in Florida and found this loss to be about 2% of the total carbon fixed. Extrapolation of the magnitude of loss from the subtropical species to eelgrass in Izembek Lagoon is at the least reasonable. Carbon is also lost in respiration, which is usually assumed to be the same in the light as in the dark, but increasing evidence suggests that respiration may be reduced in the light and that efficient refixation of respired CO2 occurs in submerged plants in the light (Wetzel and Hough, 1973). On the other hand, Hough (R.A. Hough, personal communication) has found some evidence for photorespiration in the seagrasses Cymodocea sp. and Halophila ovalis. The result of this process is an increased loss of CO2 in the light and an effective reduction in the efficiency of photosynthesis. In spite of the possible errors described above the productivity of eelgrass is very high compared to other marine primary producers. It is probable that the total annual production is on the order of 1000-l 500 g C/m’, a quantity more than five times that of the phytoplankton in the North Pacific (KoblentsMishke, 1965). The productivity rates measured in this study compare closely with those fron other studies using other techniques. In a recent review of productivity data If seagrasses, McRoy and McMillan (in press) considered 4 g C/m’ per day an average rate for tropical as well as temperate species. The average rate from the present study is 4.8 g C/m2 per day, a surprisingly comparable rate, that once again confirms the view of seagrasses as one of the most productive ecosystems in the sea.
137
The kinetic analysis of carbon uptake as a function of light yields a quantitative expression that can be used to estimate eelgrass productivity under any conditions from ambient light measurements. The kinetic constants, however, are associated with considerable variability and need further documentation for eelgrass as well as other species. The light half-saturation constant (KLt) measured for eelgrass is very close to those observed for nitrogen uptake by phytoplankton in eutrophic waters (MacIsaac and Dugda.le, 1972) and this coincidence suggests a functional relationship for photosynthetic marine organisms. ACKNOWLEDGEMENTS
The technical assistance in field and laboratory of Tom Leue and Sally Dunker were invaluable to this study. The research is a part of studies of seagrass ecosystems supported by the Oceanography Section (Grant GA 30980) and the office of the International Decade of Ocean Exploration (Grant GX 37852) of the National Science Foundation. REFE:RENCES Brylinski,
M., 1971.
Release
of Dissolved
Organic
Matter
by Marine
Macrophytes.
Disserta-
tion, Dept of Zoology, Univ. of Georgia, Athens, 90 pp. Dillon, C.R., 1971. A Comparative Study of The Primary Productivity of Estuarine Phytoplankton and Macrobenthic Plants. Dissertation, Dept Botany, Univ. North Carolina, Chapel Hill, N.C., 112 pp. GrQntved, J., 1958. Underwater macrovegetation in shallow coastal waters. J. Cons. Int. Exp. Mer., 24( 1): 32-42. Hartman, R.T. and Brown, D.L., 1967. Changes in composition of the internal atmosphere of submerged vascular hydrophytes in relation to photosynthesis. Ecology, 48(2): 252-258. Koblents-Mishke, O.I., 1965. Primary production in the Pacific. Oceanology, 5(2): 104-116 Machaac, J.J. and Dugdale, R.C., 1972. Interactions of light and inorganic nitrogen in controlling nitrogen uptake in the sea. Deep-Sea Res., 19: 209-232. McRoy, C.P., 1966. Standing Stock and Ecology of Eelgrass (Zostera marina L.) in Izembek Lagoon, Alaska. Thesis, Univ. Washington, Wash., 138 pp.
McRc,y, C.P., 1970.
Standing stocks and related features of eelgrass populations in Alaska. J. Fish Res. Bd Canada. McRoy, C.P. and McMillan, C., in press. Productivity and physiological ecology of seagrasses. In: C.P. McRoy and C. Helfferich (editors), Seagrass Ecosystems: A Scientific Perspective, M. Dekker Inc., New York, N.Y. Vollenweider, R.A. (Editor), 1969. IBP Handbook. A Manual on Methods for Measuring Primary Production in Aquatic .Environments. 224 pp. Wetzel, R.G. and Hough, R.A., 1973. Productivity and role of aquatic macrophytes in lakes: an assessment. Pol. Arch. Hydrobiol., 20(l): 9-19.