IMPACT OF ESTUARINE BENTHI C
ALGAL PRODUCTION ON DISSOLVED
NUTRIENTS AND WATER QUALITY I N
THE YAQUINA RIVER ESTUARY ,
OREGON
BY,
.iONATI-IAN H. GARBER,
JOHN L. COLLINS, JR . ,
AND
MICHAEL W. DAVIS
WATER RESOURCES RESEARCH INSTITUTE .
OREGON STATE UNIVERSITY
CORVALLIS, OREGON
WRRI-112
JUNE 1992 .
IMPACT OF ESTUARINE BENTHIC ALGAL PRODUCTION ON DISSOLVE D
NUTRIENTS AND WATER QUALITY IN THE YAQUINA RIVER ESTUARY ,
OREGON
by
Jonathan H . Garber, John L . Collins, Jr ., and Michael W . Davis
College of Oceanography, Oregon State University an d
Mark O . Hatfield Marine Science Center, Newport, Orego n
Final Technical Completion Repor t
Project Number G928-04
Submitted to
United States Department of the Interior
Geological Survey
Reston, Virginia 22092
Project Sponsored by
Oregon Water Resources Research Institut e
Oregon State University
Corvallis, Oregon 9733 1
The activities on which this report is based were financed in part by the Department o f
the Interior, U . S . Geological Survey, through the Oregon Water Resources Researc h
Institute .
The contents of this publication do not necessarily reflect the views and policies of th e
Department of Interior, nor does mention of trade names or commercial product s
constitute their endorsement by the United States Government .
WRRI-112
June 1992
ABSTRACT
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Seasonal patterns of sediment community metabolism and ne t
sediment-water nutrient fluxes were investigated at two intertidal site s
on the south shore of the Yaquina River Estuary in Oregon . Ne t
sediment-water exchanges of oxygen, nitrate, nitrite, ammonium ,
dissolved organic nitrogen, and phosphate were determined using in sit u
metabolic chambers . A fully crossed two-by-two experimental design wa s
employed to examine the influences of light and the presence o f
sediment-associated macroalgae on community metabolism and nutrien t
exchanges . Chambers were deployed at each site five times during th e
period from September 1984 to July 1985 .
Complex interactions of tides, photoperiod, and climate contribute d
to considerable within-site and between-site variability in metabolis m
and nutrient exchanges in the the intertidal sediment community . B y
convention, negative fluxes indicate net removal of a constituent fro m
the water, positive fluxes indicate net flux into the water . Tota l
sediment community metabolism, measured as dissolved oxygen flux in th e
metabolic chambers, ranged from -10 to 49 mg-at 0 m- 2 h-1 . These rate s
of sediment metabolism fall well within the range reported for othe r
coastal systems . macroalgae . Net fluxes of dissolved inorgani c
nitrogen (DIN = nitrate + nitrite + ammonium) ranged from -380 to 27 0
Ug-at N m- 2 h -1 . Considerable within-site variability in sediment-wate r
fluxes could be attributed to the presence of macroalgae on th e
mudflats . Phosphate fluxes on the mudflats ranged from -15 to 54 ug-a t
Net fluxes of dissolved organic nitrogen (DON) ranged -1 . 6
P m -2 h-1 .
to 2 .5 mg-at N m -2 h -1 and exhibited the least within-site and between site variability .
The carbon :nitrogen ratio of intertidal macroalgae at our stud y
sites ranged from seasonal lows of 6-7 in mid-winter, to highs of 8-1 0
in fall . The nitrogen content of the macroalgae appeared to reflec t
changes in the abundance of inorganic nitrogen in Yaquina Bay waters .
At no time, however, did the C :N ratio of the macroalgae indicat e
nitrogen-limited growth conditions .
As expected, net fluxes of oxygen were strongly correlated wit h
light at both sites . Fluxes of nutrients, however, exhibite d
significant between-site differences . Variations in fluxes could b e
attributed to temperature at one site, while fluxes at the other sit e
appeared to be responding more strongly to light and the presence o f
macroalgae .
Fluxes of nitrogen and phosphorus, relative to oxygen, sugges t
sinks of both these elements in the intertidal community . Fluxes of
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inorganic nitrogen were one-half or less of what would be expected a t
the measured rates of oxygen fluxes . Loss of nitrogen via microbial
denitrification appears to be the most likely mechanism for the loss o f
fixed nitrogen from the intertidal sediment-water system . The mechanism
producing high 0 :P ratios in the sediment-water fluxes is not known .
Whatever the mechanism, the apparent losses of both nitrogen an d
phosphorus resulted in net changes of these elements close to the
predicted ratio of 16 :1 .
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Comparisons of nutrient sources and sinks in the Yaquina Rive r
Estuary indicate that intertidal macroalgae can be a significant sink o f
inorganic nitrogen and phosphorus during the summer and fall . Our
results suggest that during their growth season (June-October) ,
macroalgae could remove from 40% to 58 times the amount of nitrate, an d
from 23% to 218 times the amount of phosphate supplied to the estuar y
via riverflow and sediment remineralization . Dissolved nitrate in th e
Yaquina River appears to be the major source of inorganic nitrogen t o
estuarine waters . A major source of phosphorus in the estuary appear s
to be the temperature-dependent flux of remineralized phosphate fro m
both intertidal and subtidal sediments .
41
Better estimates of natural and anthropogenic nutrient inputs,
subtidal and intertidal sediment-water fluxes, macroalgal biomass, and
algal coverage are needed to construct a more tightly-constrained
nutrient budget for the Yaquina Estuary . Nonetheless, our calculations %
clearly point toward the importance of macroalgae and intertida l
sediment-water exchanges as terms to be included in the nutrient balanc e
sheet of the Yaquina Estuary .
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FOREWOR D
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The Water Resources Research Institute, located on the Oregon Stat e
University campus, serves the Stat e of Oregon .
The Institute fosters,
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encourages and facilitates water resource s research an d education,
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u bar
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beneficial use . The Institute administers and coordinates statewide a
' u if
regiona l programs of multidisciplinary research in water and related lan '! p . •
resources . The Institute provides a necessary communications an d
coordination link between the agencies of Ideal, state and fe d
government, as well as tlii private sector, and the broad r
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community at universities in the state on matters of waiver .elM, dl :
research . The Institute also coordinates the interdisciplinary ptiof graduate education in water resources at Oregon State University .
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It is Institute policy to mak e available the results of significant ..
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water-related research conducted in Oregon's universities and colle 'O ;. -, ~} }
The Institute neither endorses nor rejects the findings of'•eITe
wtlod:O•ot=
such research . It does recommend careful consideration of the- accumulated facts by those conceirred with the solution of water- r► 1
problems .
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ACKNOWLEDGEMENT S
We thank Dr . C . David McIntire for the generous loan of th e
metabolic chambers and use of the boat Synedra .
Many thanks also go t o
Lynne Krasnow and Margaret O'Brien for help "above and beyond the call "
in the field and laboratory . We thank Doug Introne for additional hel p
in the laboratory . We are deeply indebted to Dr . Andrew Carey, Jr . wh o
graciously provided office space and use of his computer for dat a
analysis and plotting . We thank Jim Butler : without his help in th e
laboratory, his computer, software, and grey natter, work-up of ou r
nutrient data would have been infinitely more difficult . Hal Batchelde r
assisted transferring data between various otherwise incompatabie micro computers .- Assistance with the statistical analyses was provided b y
consultant Susie Maresh of the Computer Center at Oregon Stat e
University . This work was suLpported by grant number G928-04 from th e
Water Resources Research Institute, Oregon State University, Corvallis ,
Oregon .
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TABLE OF CONTENTS
Pag e
ABSTRACT
FOREWARD
ACKNOWLEDGEMENTS
TABLE OF CONTENTS
LIST OF FIGURES
LIST OF TABLES
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REGIONAL WATER QUALITY PROBLEMS ADDRESSED '
1 .1 Eutrophication of Pacific Northwest Estuaries
1 .2 Relation To WRRI Research Priorities 2. RESEARCH OBJECTIVES3. RELATED RESEARCH
3 .1
Estuarine Eutrophication
3 .2 Intertidal Sediment-Water Exchange Dynamics
3 .3 Impacts of Macroalgae on Intertidal Sediment Water Fluxes 4. METHODS AND PROCEDURE S
4 .1
Description of the Study Area
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4 .2 Field Procedures
4 .3 Laboratory Procedures
5. PRINCIPAL FINDING S
5 .1
Seasonal Cycles of Environmental Parameters, . Algal
Biomass, and Intertidal Sediment-Water Exchange s
5 .1 .1
Environmental parameters
5 .1 .2 Macroalgal biomass, carbon, and nitrogen '
content
5 .1 .3 Sediment-water fluxes
5 .2 Within-Site and Between-Site Variability :
5 .2 .1 Temperature effect s
5 .2 .2 Summary
5 .3 Nutrient Flux Stoichiometry
5 .4 Influence of Macroalgae on Intertidal Nutrien t
Exchanges
5 .5 Nutrient Removal Capacity of Intertidal Macroalgae 6. CONCLUSIONS 7. LITERATURE CITED
APPENDIX 1 . Ranges and means of environmental condition s
measured during chamber deployments APPENDIX 2 . Mean sediment-water fluxes calculated fro m
duplicate treatments during each chamber deployment APPENDIX 3 . Summary of data used in nutrient supply and remova l
calculations . .:
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LIST OF FIGURE S
Page :
Figure 1 .
Bathymetry and study sites in YaquinA Bay 1 4
Figure 2 .
Environmental conditions at Sites 1 and 2 durin g
intertidal flux chamber deployments
1 9
Figure 3 .
Seasonal biomass of macroalgae in Yaquina Bay 21
Figure 4 .
Changes in ratios of carbon to nitrogen (weight%) i n
macroalgal tissue taken from chamber deployments 21
Sediment-water flux of nitrate, ammonium, and DIN in dar k
chambers without macroalgae 28
Relationship between dissolved inorganic nitrogen flu x
and temperature at Site 1 and Site 2 for all treatments . .
29
Relationship between phosphate and dissolved oxyge n
fluxes and temperature with both sites combined 30
Examples of element relationships derived from fluxe s
under various conditions 36
Comparisons of net influence of macroalgae on inorgani c
nitrogen fluxes 41
Figure 5 .
Figure 6 .
Figure 7 .
Figure 8 .
Figure 9 .
Figure 10 . River supply of nitrate (A) and phosphate (B) compared t o
calculated macroalgal removal capacity 45
LIST OF TABLES
Page
Unit area production and components of total dail y
system production of carbon, nitrogen, and phosphoru s
during August and December in two Oregon estuaries 11
Environmental conditions recorded during samplin g
from September 1984 to July 1985
18
Table 3 .
Sediment-water flux ranges and means
23
Table 4 .
Coefficient of variation of fluxes 25
Table 5 .
Analysis of variance
26
Table 6 .
Correlation matrix for Site 1
sites combined (C)
Table 1 .
Table 2 .
(A), Site 2 (B), and both
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Table 7 .
Ratios of elements calculated from flux measurements 35
Table 8 .
Matrix showing the inverse relationship between intertida l
community metabolism and the effect of sedimentrassociate d
macroalgae on sediment-water exchanges of dissolve d
inorganic nitrogen
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IMPACT OF ESTUARINE BENTHIC ALGAL PRODUCTION ON DISSOLVED NUTRIENT S
AND WATER QUALITY IN THE YAQUINA RIVER ESTUARY, OREGO N
1 . REGIONAL WATER QUALITY PROBLEMS ADDRESSE D
1 .1 Eutrophication of Pacific Northwest Estuarie s
The availability of fertilizing inorganic nutrients i s
unquestionably a first-order natural feature that contributes to th e
high productivity of estuarine ecosystems . With continued developmen t
of estuarine basins, inputs of nutrients from sewage, agriculture, an d
other land uses become increasingly important terms in estuarin e
nutrient budgets . The response of estuaries to increasing nutrien t
loadings are very poorly understood . Unlike many freshwater system s
where responses to dissolved nutrients (phosphorus, in particular) ar e
well documented (see e .g, Jaworski 1981, Ryther and Officer 1981, Nixon
and Pilson 1983), the ability of estuarine systems to absorb increase d
nutrient inputs without the deleterious effects of overfertilization i s
not known .
Much of the available information on estuarine nutrient dynamics i n
the United States comes from East and Gulf coast studies . Relativel y
little is known about estuarine systems of the Pacific Northwest .
Fundamental differences in regional climate, underlying geology ,
hydrography, and watershed usage suggest that paradigms of nutrien t
loading developed for other coastal regions may be inappropriate i f
blindly applied to the systems of the northwest . There are, fo r
example, seventeen major estuarine systems along the Oregon coas t
(Division of State Lands 1973) .
Many of these, including the Yaquina ,
are relatively small, multi-use water bodies . Nearly all Oregon' s
estuaries receive freshwater from streams and rivers that drai n
sparsely-populated forested watersheds of coastal mountains . Seasona l
patterns of dissolved nutrients in the Yaquina River Estuary (J . Garber ,
unpub . data) show that large amounts of nitrates-nitrogen are introduce d
at the riverine end of the estuary following the onset of the winte r
rains . The source and fate of this nitrate are not known . However ,
considerable research has shown that the primary production of estuarin e
and coastal waters is often limited by the availability of inorgani c
nitrogen (Ryther and Dunstan 1971 and others) . Thus the influx o f
nitrate from coastal rivers, along with other natural and anthropogeni c
sources of nutrients may be contributing to the progresq ;i :ve
eutrophication of this estuary . The impact of this enr.iohment is no t
known . Nutrient enrichment could enhance estuarine primar y
productivity, which in turn could support larger populations of finfish ,
shellfish, and birds . However, it is impossible to predict the • =level of
loading that will result in over-enrichment, or eutrophication, .p . the
system without quantitative measurements of nutrient sources and sink :.
1 .2 Relation To WRRI Research Prioritie s
Intertidal regions (mudflats and sandflats) comprise an average o f
about 46% of Oregon's total estuarine area (Oregon Department of Stat e
Lands 1973) .
This project assessed the role of some typical intertida l
areas as sources, sinks, and transformers of dissolved inorgani c
nutrients in the Yaquina River Estuary . This research addressed th e
following specific problems identified as priority areas for WRRI supported research, 1984-1987 :
Protection of bay, estuarine and wetlands resources . Increase d
nutrient loading may initially lead to increased biologica l
productivity . Eventually, the input must exceed the uptake an d
recycling capacity of indigenous estuarine populations . The
consequences of eutrophication--anoxic conditions, reduced productivit y
of desirable estuarine fish and shellfish, degradation of wildlif e
habitat--have been well documented in freshwater and marine systems .
Impact of land and ocean use on coastal water quality . We have
documented the dramatic increase in dissolved nitrate in the Yaquin a
River Estuary that accompanies the increase of streamflow with the onse t
of winter rains . Although the source of this nitrate is not known w e
hypothesized it originates in the watersheds of the coastal rivers . I f
this hypothesis is correct, land use in the watershed could b e
contributing to estuarine eutrophication . The impact of this enrichmen t
is unclear . This project was designed to assess how much of thi s
nutrient loading could be absorbed by the intertidal component of th e
estuarine system, thus quantifying one term in the overall nutrien t
source-sink equation of the estuary .
Evaluating environmental and economic tradeoffs due to development .
Pressures for residential and commercial development of the shores an d
watersheds of Oregon's estuaries will continue and, if economi c
conditions in the state continue to improve, increase in the future .
The ability of the estuarine system to absorb increased nutrien t
loadings, and perhaps convert the loadings into harvestable species, i s
central to the question of wise and balanced resource management . I t
may, for example, be possible for an estuarine system such as th e
Yaquina to handle increased nitrogen input with no deleterious effects ;
the fertilizing effect of the river may actually contribute to th e
continued development of commercial oyster culture in the estuary . Bu t
the capacity of the system may be overtaxed if the riverine flux i s
augmented with a substantial increase of nitrogen loadings fro m
wastewater or other sources . The purpose of our proposed research was t o
assess the capacity of one component of the estuarine system, th e
intertidal benthic community, to transform inorganic nitrogen an d
phosphorus into organic matter which may be passed to higher levels o f
the estuarine food webs .
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Survival ofanadromous fishes . Siinenstad and Wismar (1983 )
recently reviewed evidence for the importance of estuarine production i n
the survival of Pacific salmon (Oncorhynchus spp .) . Juvenile chum ,
chinook and coho salmon, in particular, feed on small benthic Organism s
that occur in great numbers in intertidal mudflats . The prey of
juvenile salmon feed on benthic algae and algal detritus . Thus change s
in benthic algal production could be passed along estuarine food chain s
and contribute to the success of salmonid species .
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2 . RESEARCH OBJECTIVE S
The purpose of this research project was to assess the role o f
intertidal sediment communities in the nutrient cycling dynamics of th e
Yaquina River Estuary, Oregon . In particular, we were interested i n
determining the nutrient uptake capacity of the macroalgae, Ulva an d
Enteromorpha species, that often form dense mats over the surface o f
intertidal sediments in summer and early fall . We hypothesized tha t
macroalgal growth could remove significant quantities of dissolve d
inorganic nutrients from estuarine waters thereby transforming inorgani c
nutrients into high-quality (nitrogen-rich) organic matter . Thi s
organic matter could in turn be passed to higher levels of estuarin e
food webs as well as 'contribute to natural biological oxygen deman d
(BOD) when it decomposed . We also determined relationships betwee n
benthic algal production and the net exchange of oxygen and inorgani c
nutrients across the sediment-water interface in these intertida l
sediment communities .
The specific research objectives guiding this work were :
(1)
to determine the net fluxes of nitrate, nitrite, ammonium ,
dissolved organic nitrogen (DON), reactive phosphate, an d
dissolved oxygen between estuarine water and intertida l
sediment communities ;
(2)
to measure nutrient uptake capacity of the intertidal benthi c
macroalgae found at our study sites ;
(3)
to examine relationships among intertidal community metabolis m
benthic macroalgal production, and net fluxes of nutrient s
across the intertidal sediment-water interface ; an d
(4)
to determine whether intertidal communities act as net seurt•e s
or sinks of inorganic nutrients at the current levels o f
nutrient loading in the Yaquina estuary .
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3 .1
RELATED RESEARC H
Estuarine Eutrophicatio n
Understanding and controlling the fate and effects of pollutants i n
estuarine ecosystems remains a problem of global proportions . Althoug h
an impressive amount of quantitative data on a host of pollutin g
substances introduced into estuaries is now available, our ability t o
predict and mitigate adNcerse effects of these substances remain s
limited . Case studies, such as those for the Clyde Estuary (Macay an d
Leatherland 1976), Burry-Inlet (Chubb and Stoner 1977) in Great Britain ,
and the Hudson River Estuary in this country (Malone 1984), ampl y
illustrate the adverse changes in water quality and biological resource s
brought about by anthropogenic inputs of nutrients, toxic chemicals, an d
sediments . Such adverse effects include degradation of recreatio n
areas, loss of shallow-water fisheries, loss of the estuary as a nurser y
for offshore fisheries, and blockage of migratory corridors fo r
anadromous fish (Chubb and Stoner 1977) .
Evidence for the increased nutrient loading of estuaries an d
coastal waters (e .g ., Jaworski 1981, Walsh et al . 1981, Meybeck 1982 ,
U .S. EPA 1. 982) leave little question about the ultimate anthropogeni c
source of the problem . Sewage now accounts for 50% or more of th e
inorganic nitrogen loading of Long Island Sound, New York Bay, Rarita n
Bay, Delaware Bay, and San Francisco Bay (Nixon and Pilson 1983) .
Problems attending the eutrophication of estuaries may b e
exacerbated by the retention of riverborne material within the estuary .
The notion of estuaries as "filters"' between the land and the sea ha s
received a great deal of attention, especially by sedimentologists, an d
this very topic provided the focus of a recent symposium (Kennedy 1984) .
The combination of physical, chemical, and biological processes tha t
occur when fresh and salt waters mix contributes to the trapping o f
material within an estuary (Sharp et al . 1984) . For example, riverborn e
material may be removed from solution near the head of an estuary b y
flocculation in the "turbidity maximum" zone of the salinity gradient .
Farther downstream, active uptake of substances from solution b y
estuarine organisms may have a significant i-mpact on estuarine wate r
chemistry (Kaul and Froelich 1984) .
The effectiveness of the estuarin e
filter in terms of trapping introduced material is therefore determine d
by numerous site-specific physical, chemical, and biological factor s
(Schemel et al . 1984) .
At the same time, and further complicating an y
simple rendition of estuarine function, estuaries are thought to expor t
or "outwell" nutrients to offshore waters (Odum 1971) .
The disparit y
between these two seemingly opposite aspects of estuarine functio n
illustrates the limits of our understanding of these systems (Nixon 1981) .
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Although estuaries and freshwater lakes may exhibit some simila r
responses to nutrient enrichment, the causes and mechanisms of th e
enrichment are often quite different . Algal production in temperat e
freshwater lakes is often limited by the availability of phosphoru s
(Shindler and Fee 1973) .
Eutrophication of these waters can therefor e
often be attributed to the introduction of excess dissolved phosphate .
Primary production in coastal marine waters, however, is thought b e
limited by the availability of inorganic nitrogen (Ryther and Dunsta n
1971, Shindler 1981, Jaworski 1981) .
Along the estuarine transitio n
from fresh to salt water we might expect to find a parallel transitio n
from phosphorus to nitrogen as the primary limiting nutrient . Although
this particular aspect of the problem has not received much attention ,
the productivity of the . more saline reaches . of many estuaries is ofte n
nitrogen-limited (Ryther and Dunstan 1971, Smayda 1974) .
3 .2
Intertidal Sediment-Water Exchange Dynamic s
Sediment communities, now recognized as integral parts of coasta l
ecosystems, are coupled to the surrounding waters by flows of energy al6d
nutrients . Secondary production of the benthos is to a large exten t
dependent on the primary production of the overlying water (Zeitzs0hel.' 1980) . At the same time, heterotrophic processes in the sediments &e :t
to replenish the inorgahic nutrients needed to support pelagic primar y
production (Boynton et al . 1980, Nixon 1981) .
The significance of such sediment-water exchanges had long bee n
recognized in lakes (e .g ., Mortimer 1941) .
Investigation of these . a
processes in estuaries and coastal waters began in earnest only abow t
ten years ago [Nixon 1981 ; Okuda's (1960) remarkable and ofte n
overlooked work on Matsushima Bay is a notable exception] . High hate s
of metabolic activity, usually measured as sediment oxygen demand. 0040
have been found in many types of coastal marine sediments (Zeitzsehel .
1980) . The connection between benthic metabolism and nutrient .ii lin g
has become an area of active research . For example, Nixon (1981) foun d
a linear relationship betweai annually-averaged rates of total be rth4 e
metabolism and the amounts of organic matter introduced into a variet y
of coastal systems . His regression, which predicts that about 25% o f
the organic carbon entering an estuarine system is consumed by benthi c
communities, has been supported by recent analysis of data fro m
Chesapeake Bay (Officer et al . 1985) .
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Stoichiometric relationships between metabolic processes and
nutrient cycles in seawater and sediment are often presented in . terms o f
"Redfield ratios" (Redfield et al . 1963) .
This model predicts,i.ttva t
aerobic and anaerobic respiration in marine waters and sediments' • W.il l
produce carbon dioxide and inorganic ("remineralized") forims, of- TUtr®g n
and phosphorus . High levels of sediment m,tabolic activity have been
found to be accompanied by the accumulation of remineralized nutrient s
in sediment interstitial waters (McCaffrey et al . 1980, Klump an d
Martens 1981, and others) . Sediments therefore represent a potentiall y
important reservoir of remineralized nutrients . Strong concentratio n
gradients between sediment interstitial and overlying waters lead to th e
diffusion of nutrients into the overlying water . Burrowing and feedin g
activities of benthic organisms also contribute to the flux of nutrient s
to the overlying water (McCaffrey et al . 1980) .
A useful measure of the contribution of nutrients from sedimen t
communities to the nutrient budget of an estuary can be gotten by
comparing the magnitude of the benthic flux to the amount of nutrient ,
usually nitrogen, needed to support annual primary production in th e
estuary . A list of such data for diverse coastal systems, compiled by, _
Nixon (1981), shows that benthic nutrient remineralization often
accounts for 25% to 50% of the nitrogen required for plant production ,
in some cases supplying more than the total annual nitrogen requirement .
The literature now contains many measurements of sediment communit y
metabolism (Zeitzschel 1980) . Reports of sediment nutrient fluxes hav e
been reviewed by Nixon (1981) . Most of these studies were restricted t o
subtidal sediment communities, and nearly all dealt exclusively with th e
heterotrophic components of the sediment system . A few measurements of
both sediment metabolism and nutrient fluxes are available for shallo w
(less than a few meters depth) marine communities . For example, Nowick i
and Nixon (1985a, 1985b) examined sediment metabolism and nutrient flu x
dynamics in a shallow temperate marine lagoon . Welsh (1980) attempte d
to quantify nutrient exchanges between Long Island Sound waters and a
marsh-mudflat system in Connecticut . We know of no work, comparable t o
that reported here, dealing with sediment metabolism, nutrient fluxes ,
and autotrophic processes in an estuarine intertidal community .
3 .3
Impacts of Macroalgae on Intertidal Sediment-Water Fluxe s
The functional role of benthic macroalgae in the energy an d
nutrient budgets of estuarine systems has not yet been examined in grea t
detail (Kemp et al . 1982) . Macroalgal standing stocks in estuarie s
range from 100-500 grams dry weight (gdw) m -2 (Conover 1958, McComb e t
al . 1981, Owens and Stewart 1983, Thom 1984) . The high biomass o f
these plants, coupled with their high potential rates of productio n
(Kremer 1981) suggest that they might have significant impact o n
estuarine nutrient cycles . A strong link between benthic alga l
production and fluxes of nutrients from sediment to the water column ha s
in fact been suggested by Welsh (1980) and Kautsky (1982) . Benthi c
algae assimilate nutrients during the growing season, acting as a ne t
sink of inorganic nutrients while algal biomass is increasing . Locate d
at the sediment-water interface, intertidal plants are ideally situated
t
to intercept the benthic flux of remineralized nutrients . Dissolved an d
particulate forms of the nutrients may then add to the total flux o f
remineralized nutrients as the algae senesce and die (Owens and Stewar t
1983, Pregnall 1983) .
Evaluation of the impact of intertidal macroalgae on estuarin e
nutrient dynamics requires knowledge of algal distributions, production ,
and influences on net sediment-water nutrient exchanges . Previou s
research has demonstrated-that that macroalgae are abundant in man y
coastal ecosystems (Sawyer 1966, Mann 1973, Fitzgerald 1978, McComb
al . 1981, ShMllem and Josselyn 1982), and that the primary productivit y
of macroalgal assemblages can reach 1000 g C m -2 y -1 (Ryther 1959, Man n
1973, Thom 1984) . The production cycle of most benthic macroalgae i s
strongly seasonal and apparently controlled by complex interactions o f
environmental conditions such as light intensity, temperature, an d
inorganic nutrient supplies (Conover 1958) . On the global scale, Smith
(1981) estimated that that benthic macroalgal production represented a
significant carbon sink, amounting to some 10 9 tons of carbon annually ,
or about 5% of phytoplankton production of the world ocean .
et
In the Pacific Northwest,- mid-summer biomass of the two most .
common estuarine intertidal macroalgal species, Enteromorpha prolifer' a
and Ulva expansa, often exceeds 400 gdw m -2 (Davis 1981, Thom 1984) . I t
is not known whether the intertidal community, when its effects ar e
integrated over an entire growing season, serves as a net source or sik k
of dissolved inorganic nutrients . To gauge the potential importance o f
macroalgal production we assembled preliminary nutrient budgets tw o
Oregon estuaries (Table 1) .
We assumed similar daily rates of ne t
production in both systems and estimated (by planimetry based on fie d
surveys) that 30-40% of the total area of these estuaries represents ;*
habitat suitable for macroalgal growth . The calculations summarized , i n
Table 1 indicate that benthic macroalgae may be responsible for at leaS:t
one half of the total plant production of these systems in summer . I h
winter, macroalgal production drops to nearly zero, and the fractiop,o f
production attributable to the other producers rises proportionately.:
As illustrated in Table 1, benthic macroalgal production coul d
represent a significant demand for inorganic nutrients . Assumin g
Atkinson and Smith's (1983) average macroalgal composition of 550 :30 : 1
(C :N :P) and a reasonable production rate of 50 moles C m -2 y -1 , w e
estimated that macroalgal production represents a demand of some 2 .7
moles N m -2 y -1 ,
and about 0 .09 moles P m -2 y- 1 . No annually
.
integrated sediment flux data have been reported for an intertida l
community . However, Nowicki et al .'s (19,85a, 1985b) studies of ski tida l
benthic nutrient fluxes in a shallow coastal lagoon- provides some basi s
for comparison . The net flux of remineralized nutrients from th e
coastal pond sediments could supply only 10% or less of the nit r'ogen
'
an d
phosphorus required for our calculated rates of intertidal . .ma•e .rophyte prodTi tion .
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4.
METHODS AND PROCEDURE S
4 .1 Description Of The Study Are a
Our investigations of intertidal sediment-water flux dynamics wer e
carried out at two sites located in lower reaches of the Yaquina Rive r
Estuary, Oregon (Figure 1) . The Yaquina Estuary lies at the mouth of
the Yaquina River, a relatively small coastal Stream that drains a
watershed of some 627 km 2 in west-central Oregon . Discharge of Yaquin a
River, gauged since 1972 (Friday and' Miller 1984), is strongly seasonal .
Peak flows of 1000 cubic feet per second (cfs) generally occur in earl y
winter (November-December) while minimum flows Of 10 cfs or less occu r
in late summer (August-September) . The ten-year-(1972-1982) mea n
discharge of the river was 251 cfs . The estuarine portion of the rive r
extends about 30 km inland from the Pacific Ocean . The estuary occupie s
an area of 3910 acres, of which about 35% (1353 acres) is classified a s
tidelands (Oregon Division of State Lands 1973) . A dredged shippin g
channel, 15-20 m deep, extends about 5 km inland from mouth of th e
estuary ; mean water depth 'of the estuary as a whole is about 4 m . The
estuary is subject -to the mixed, semidiurnal tide of the Pacifi c
Northwest coast ; average tidal range near the mouth of the estuary i s
2 .4 m, maximum spring tidal range is 3 .8 m . Tidal exchanges of water far .
outweigh the influence of riverflow in structuring the water column .
Ratios of freshwater dischargd•to the tidal prism range from 0 .002 t o
0 .3 . The combination of shallow depths, generally low freshwater input ,
and vigorous tidal mixing produce well-mixed conditions throughout th e
estuary during most of the year (Burt 1956, Burt and McAlister 1959) .
Temporary vertical salinity gradients occur during winter freshets .
Sediment-water flux determinations were carried out at tw o
locations on the south shore of the estuary (Site 1 and Site 2, Figur e
1) . Sediments at Site 1, were classified by Kulm (1965) as fine, mediu m
and silty sands with an organic matter content of about 3% ; those a t
Site 2 were classified as silty sands with very low organic content .
Phi medium diameter of the sediments at both sites ranged from 2 .3 t o
3 .6 (Kulm 1965) . Both sites were characterized by luxuriant growths o f
sediment-associated macroalgae, and we assumed a priori that Sites 1 and
2 represented ocean-dominated and river-dominated intertidal systems ,
respectively .
4 .2 Field Procedure s
The net flux of inorganic nutrients and benthic productivit y
measurements were performed in situ using a stirred "bell jar" approach .
Recent applications of this technique were reviewed by Zeitzschel (1980) .
Details of the construction of the chambers used in this study wer e
described by Davis (1981) . Each experimental set consisted of four
chambers (two light and two dark) for each of two treatments : (1) intac t
sediment community including naturally-occurring densities o f
macroalgae ; and (2) sediment community minus macroalgae -- all visibl e
forms of macroalgae either absent or removed by hand . During chambe r
deployments we also incubated four 1 :-liter bottles (two light and tw o
dark) containing samples of macroalgae in coarse-filtered (50pm) ba y
water and four 1-liter bottles (two light and two dark) containing onl y
coarse-filtered bay water . The eight bottles were suspended in th e
water near the sediment surface so that, like the chambers, they wer e
exposed to ambient light and temperature .
The chambers were deployed about 2 hours before high slack tide o n
days when the higher high tide occurred within one hour of local noon .
Each chamber was pressed about 30 cm into tbe-_pediment enclosing 129 c m 2
of sediment surface . Ambient bay water was admitted to the chamber s
through a small port in the chamber wall . When full, initial wate r
samples were taken from the 5 .7 liters of bay water enclosed in th e
chamber over the sediment . This water was replaced with ambient ba y
water . The chambers were then sealed . The water over the cores wa s
gently stirred during incubation by a battery-powered impeller . Th e
chambers were completely submerged during the incubation period . Fina l
water samples were taken from the chambers about two hours after hig h
slack tide . Water samples for dissolved oxygen were taken in the fiel d
in 300 ml or 60 ml BOD bottles and "fixed" immediately for azide modified Winkler titrations (Golterman et al . 1978) . Nutrient sample s
were taken in specially-cleaned polyethylene bottles and kept on ice .
Macroalgae present in the chambers and bottles were removed at the en d
of the incubation periods rinsed with clean bay water, wrapped i n
aluminum foil and returned to the laboratory on ice .
Mid-winter higher high tides occur at night, rather than during th e
day, thus making it impossible for us to carry out the deployments i n
the field . Therefore on two occasions (December 3 and January 12) ,
sediment samples were taken at low tide and carried back in thei r
respective chambers to the laboratory in Newport . The chambers wer e
placed in large outdoor tanks and supplied with a continuous flow of ba y
water . Flux determinations were then carried out the next day usin g
procedures essentially the same as those used in the field .
Environmental data were collected hourly on site during eac h
chamber deployment . Water salinity, temperature, and depth wer e
determined using a submersible conductivity-thermistor probe (Montedoro Whitney CTU-3) . Surface and bottom light intensity, measured photo n
flux of photosynthetically active radiation (PAR), was determined usin g
a LiCor integrating quantum photometer with a spherical (4-pi) sensor .
ti
-15 -
4 .3
Laboratory Procedure s
Nutrient samples, returned to the laboratory on ice in dar k
coolers, were immediately filtered (Whatman GF/C) and split fo r
automated nutrients (nitrate, nitrite, and phosphate), ammonium, an d
dissolved organic nitrogen (DON) determinations . The salinity of th e
nutrient split was checked with an American Optical hand-hel d
refractometer . Oxygen titrations (Strickland and Parsons 1972) an d
ammonium determinations (Solorzano 1969) were carried out within 2 4
hours . The remaining nutrient and DON samples were stored frozen i n
acid- and acetone-washed polyethylene bottles for 2 days to 2 week s
before analysis . Dissolved nitrate, nitrite, and phosphate were the n
determined by standard automated procedures using an Technicon AAI I
system (Strickland and Parsons 1972) . DON was determined by persulfat e
digestion (D'Elia et al . 1977) modified by us for an automated finish .
Samples of macroalgae from the chambers were rinsed briefly i n
deionized water, frozen in liquid nitrogen, freeze dried, weighed, an d
ground by hand to a fine powder . The carbon and nitrogem conte,mt of the
freeze-dried samples was determined by high-temperature combustio n
(Perkin-Elmer 240 Elemental Analyzer) .
The net fluxes of oxygen and nutrients across the sediment-wate r
interface were calculated by differences between initial am-0 fina l
concentrations of the constituents in the water over the sediments ._
Negative fluxes indicate net removal of a constituent from the wate r
column (presumably into the sediment or algae) while positive fluxe s
indicate release of a constituent to the water column . Flux
calculations included terms for chamber volume,'sediment area, and ba y
water controls . Estimates of net community production and respiratio n
were based on oxygen changes in the light and dark chambers ,
respectively .
5.
PRINCIPAL FINDING S
5 .1
Seasonal Cycles of Environmental Parameters ,
Algal Biomass, and Intertidal Sediment-Water Exchange s
5 .1 .1
Environmental parameters .
Variability is a distinguishing characteristic of estuarin e
environments . Intertidal estuarine habitats, in particular, are slAWjec t
to the interacting diel cycles of sunlight and tides, the longor•peie!io ;d '
cycles in photoperiod, air and water temperature, as well as shifts i n
salinity and water chemistry due to variations in riverflow and the' direct effects of precipitation . The intertidal environment = is- ,
therefore subjected to considerable diel and seasonal ranges of ligb t
intensity, temperature, salinity, and nutrients . Some indidators of
this variability are reflected in the range of environmental condition s
found at our study sites (Table 2, Figure 2) . A complete record o f
these data is given in Appendix 1 .
Environmental conditions on the tidal mudflats followed typica l
temperate patterns . Summer months were characterized by high ligh t
intensity, long photoperiod, and warm temperatures . Decreasing
riverflow throughout the summer and fall is reflected both in the h-ig4e r
salinities recorded over the flats as well as in the ambient dissolved .
nutrient content of the water . Freshwater entering the Yaquina Estuary .
generally contains high concentrations of nitrate and very littl e
phosphate . In contrast, the seawater entering the mouth of the estiza'r y
is relatively phosphate-rich and nitrogen-poor . Flow of the Yaquin a
River is tightly coupled to the monsoonal rainfall pattern of the Orego n
Coast (Friday and Miller 1984) .
Winter rains, beginning in late fall _
(October and November) are accompanied by increases in freshwater flo w
into the estuary and a concomitant rise in nitrate levels in estuarin e
waters . Rains and riverflow generally taper off to near zero in lat e
summer (September and October), the salinity of estuarine waters rises ,
and nutrient levels drop . These patterns are consistent with the timing
of maxima and minima of the parameters listed in Table 2 . Th e
situations is,-complicated somewhat by coastal upwelling events tha t
periodically , introduce anomalously cold, nutrient-rich waters ocea n
waters into the bay during the summer and fall . The high levels o f
phosphate found during September (Table 2) are probably attributable t o
such an event .
Differences between surface and near-bottom PAR light intensitie s
(Figure 2A), usually 5-4 iE s_1 m-2 , gave vertical extinctio n
coefficients (K) between 0 .22 and 0.61 m ` 1 , or light transmission value s
of 54-80% m -1 . The waters flooding the mudfl;a .ts were therefore rathe r
clear for an estuary . This suggests the influence of relatively clea r
ocean waters and sandy sediments -- which are not easily resuspended b y
-17 -
Table 2 : Environmental conditions recorded during samplin g
from September, 1984 to July, 1985 . Eac h numbe r
is a mean from one sampling run . Ambien t analyt e
concentrations are expressed as uM unles s
specified otherwise .
Parameter
Range
Month of Occurrenc e
Maximum
Minimum
Water temperature
(degrees ,C )
Salinity
Light (water surface)
(i'E s -1 m-2 )
Vertical Extinction
Coefficient, k (m il )
Nitrate
Ammonium
Nitrite
Phosphate
Silicate
DON (dissolved
organic nitrogen )
Dissolved oxygen
(mg-at 0 1 -1 )
8 .1-17 .9
January
Jul y
15 .4-33 .5
2 .6-20 .9
March
October
Jun e
Jun e
0 .22-0 .61
July
Decembe r
0
1
0
0
8
3
September
Decembe r
October
January
October
March
De.e.embe a
.8-32 .2
.55-4 .80
.19-0 .56
.71-1 .46
.4-99 .6
.6-7 .4
0 .386-0 .889 October
-18 -
e: r
Septembe r
Marc h
Decembe r
D e•e .eAt
Jul y
1
E
FIELD ENVIRONMENTAL CONDITION S
Light Intensity . Surface and Bottom
A.
a 30
W
a
o
q surfac e
0
°
x 20 ~'
q
+
C
C
=
o
•
+bottom
q
+
+
10 q
a
q
q
+
+
+
0
1
I
I
t
t7
r
1
r
1 I
T
I
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1
I
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~t
4
I I
I
i
B . Photoperio d
15
q
5
I
r
►
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O
q
a
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a
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i
1
q
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[
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L]
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I
C. Bottom Temperature
20
q
q
10 -
0
D
T
J
I
F
I
T
C
n
I
T
M
1985
A
0
I
M
I
1
J
I
1
J
Month
t
1
A
I
I
S
I
I
0
I
N
T
D
198 4
Figure 2 : Environmental conditions at sites 1 and 2 during intertida l
flux chamber deployments . Mean light intensity (A) and mean
bottom temperature (C) on-site . Photoperiod data (B) wer e
calculated from daylength data in Smithsonian Meterologica l
Tables Gist 1971)
tidal currents and wind waves -- in the lower reaches of the estuary . .
There was some indication that the waters flooding the mudflats wer e
clearest in early summer and most turbid in mid-winter . In general ,
however, well over 50% of the incident PAR was transmitted to th e
sediment surface at high tide during chamber deployments .
5 .1 .2 Macroalgal biomass, carbon and nitrogen conten t
Unfortunately, estimates of total intertidal macroalgal biomass i n
the Yaquina Estuary are not available . Davis (1981, and unpub . data )
has documented the seasonal changes'in dominant macroalgal species o n
mudflats in Yaquina and Netarts Bay . Davis' data from 1978-197 9
(unpub . •data) recorded Enteromorpha biomass peaking rapidly to
80 0
gdw m -2 in mid-summer (Figure 3A) then declining steadily through th e
late summer and fall . Ulva species follow Enteromorpha as the dominant
macroalga on the mudflat . Ulva biomass apparently peaks in late summe r
or early fall, but it is not uncommon to find the two genera occurrin g
together .
We estimated total macroalgal biomass per square meter-of m .udfla t
from the amount of macroalgae enclosed by our chambers . This was not - a
rigorous measure of total biomass due to the small area enclosed by th e
chamber and sampling bias . Our selection of chamber placement at eac h
site was not stratified or carefully randomized .. Even so, the pLattrnof macroalgal biomass food in the chambers was roughly similar't o
Davis' data for Enteromorpha (Figures 3A and 3B) . However, peak,bio•m*as s
in the chambers occurred later in the season and all our biomas s
estimates were considerably less than that for Enteromorpha alone . On
the other hand, we were surprised to find that some macroalgae, usuall y
Ulva spp ., were present on the mudflats throughout the winter .
The ratio of total carbon to nitrogen (C/N) in macroalgal tissue s
is a useful measure of the physiological status of the plants . C/ N
ratios over 10 are often indicative of nitrogen shortage, while ratio s
around 6, close to that of Redfield's "average marine organic matter, "
suggest that the plants have ,an adequate supply of nitrogen (Haniaa k
1983) . The C/N ratio of macroalgae recovered in our chambers range d
from mid-winter lows of about 6 .7 to early fall highs around 9 .0 (Figur e
4.4) . Although there is considerable scatter in the C/N data the tren d
follows the abundance of inorganic nitrogen in the water . Low C/N
ratios occurred during periods of highest dissolved nitrate • T
concentrations and vice versa . The relatively low C/N ratios in+dise te d
that the plants always had an adequate nitrogen supply regardless of th e
season . This, then, is another indication that the 1 atp iaa estuary g s Ai
nitrogen-rich system .
1-20 -
MACROALGAL BIOMAS S
A.
1
a
Enteromorpha app .
0 .8-•
E
p
A0
0 .6 0 .4 -
0 . 2-,
0
r
B.
140 -
a
a
T
T
t
t
i
I
I
T
Ulva app. and Enteromorpha app.
120 -c;'
E
100 -
80 a
60 -
40
20 0
1
1
F
J
1
1
1
M
1
1
A
M
Q
Q
r
I
T
J
I
T
J
1
1
A
S
l
I
0
Month
1985
r
1
I
N
D
1984
Figure 3 : Seasonal biomass of macroalgae in Yaquina Bay . A. Biomas s
of only Enteromorpha spp . at Site 1 (from Davis, unpublishe d
data) . B . Biomass of Ulva spp . and Enteromorpha spp . foun d
in chamber deployments during this study . In both figures ,
symbols indicate the mean * 1 S .D . Note difference i n
biomass scales .
MACROALGAL C/ N
6
T
J
i
F
1
1
M
1985
[
{
A
I
S
M
1
1
J
i
T
J
Month
T
I
A
1
I
S
!
{
1
0
t•t
I
1984
Figure 4 : Changes in ratios of carbon to nitrogen (weight %) i n
macroalgal tissue taken from chamber deployments . Point s
indicate mean f 1 S .E .
{
D
5 .1 .3
Sediment-water fluxe s
Deployments of sediment-water flux chambers were carried out fiv e
times at each of two intertidal study sites in the Yaquina Estuar y
between September 1984 and July 1985. Sediment-water flux data acquire d
during these experiments is summarized in Table 3 and reported in detai l
in Appendix 2 .
Not surprisingly, environmental variability on the mudflats wa s
accompanied by considerable variability in sediment-water exchanges at
each site as well as by significant differences in nutrient exchang e
processes between sites . However, some general patterns emerge from the ,
examination of the mean fluxes for each analyte during the study perio d
(Table 3).
Additional patterns were revealed by the regression an d
statistical analyses discussed in following sections .
For convenience in the following discussions, the chambe r
treatments will be referred to using the abbreviations : LW = clear
chambers containing macroalgae ; LWO = clear chambers without macroalgae ;
DW = dark chambers containing macroalgae ; DWO = dark chambers withou t
macroalgae . In later sections we will use the following shorthan d
notations : L = all clear chambers ; D = all dark chambers ; W = al l
chambers containing macroalgae ; WO = all chambers without macroalgae .
Examination of the means of fluxes at each site during the study perio d
revealed the following :
-
Net release of dissolved inorganic nitrogen (DIN = the sum-o f
nitrate, nitrite, and ammonium) to the overlying water occurre d
in the DWO chambers . This net nitrogen release was due, i n
particular, to the net release of ammonium . Nitrite, . on . th e
other hand, was generally removed from the water in the DW O
chambers . Nitratefluxes in the DWO chambers were too variabl e
between sites to warrant generalization .
Net uptake of nitrate generally took place in the LW chamber s
at Site 2 and in all L treatments at Site 1 .
-
Net flux of nitrite was generally from the water into th e
sediment or algae regardless of treatment or site .
-
Dissolved organic nitrogen (DON) fluxes-were variable, but ne t
release to the overlying water generally took place in th e
dark .
-
Net exchanges of phosphate were also variable but het releas e
from the sediment to the water generally occurred in the dar k
chambers .
1
1
L
Y
w
S
N
I
I
1
1
I
•
d m
1
m 4
1
w d
1
9 .0
1
4 6
1
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u u
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d d 00 1
uw H 1
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Net fluxes of oxygen followed expected patterns of ne t
production in the clear chambers, indicating exces s
photosynthesis over respiration, and consumption in the dar k
due to community respiration .
5 .2 Within-Site and Between-Site Variabilit y
Total sediment community metabolism, measured as changes in oxyge n
concentrations in the metabolic chambers, ranged from -10 to 49 mg-at 0
m-2 h-I (Table 3) . These rates of sediment metabolism fall well withi n
the range reported for other coastal systems . Within-site variabilit y
was estimated by calculating coefficients of variation for the mean flu x
of each constituent for each treatment at Sites 1 and 2 (Table 4) .
Greatest variability in oxygen fluxes occurred in chambers tha t
contained macroalgae . Net fluxes of DIN (nitrate + nitrite + ammonium )
ranged from -380 to 270 p g-at N m- 2 h-1 , and exhibited the greates t
within-site variability . Coefficients of variation for DIN fluxes i n
chambers containing macroalgae ranged from 93% to 466 times the mea n
flux at Sites 2 and 1, respectively . Phosphate fluxes ranged from -1 5
to 54 Pg-at P m -2 h -1 , and appeared less variable, especially in dar k
chambers (C .V ., 100-200%) . This indicates some uniformity in sediment associated phosphorus remineralization at the intertidal sites . Ne t
fluxes of DON exhibited the least within-site and between sit e
variability, giving C .V .'s for each site that ranged from 44-98% .
Analysis of variance using the four chamber treatments as factor s
and temperature as a covariate was used to further examine the between site differences in mean flux data reported in Table 3 . Although no t
all the probabilities reported in the ANOVA (Table 5) are statisticall y
significant, those close enough to merit consideration and further stud y
are discussed . The most striking result of the ANOVA is the indicatio n
of a strong relationship between temperature and DIN fluxes, includin g
nitrate fluxes, at Site 1 . In contrast, DIN fluxes and temperatur e
varied independently at Site 2 . This, of course, suggests tha t
processes controlling DIN fluxes differed significantly at the two site s
and that the primary factor controlling variations of DIN fluxes in th e
intertidal communities was not the presence or absence of macroalgae .
The ANOVA also revealed that only ammonium of all the various form s
of nitrogen seemed to vary in response to the chamber treatments at Sit e
1 . At Site 2 however, nitrate flux appeared influenced by both ligh t
and macroalgae, as well as macroalgae contributing significantly t o
variations in DIN flux .
Phosphate fluxes did not exhibit strong between-site differences .
The ANOVA indicated weak covariance of phosphate fluxes with macroalga e
at Site 1, with light at Site 2, and with temperature at both sites .
Table 4 : Coefficient of variation for fluxes . Arranged b y
treatment, by site . Abbreviations as in Table 3 .
LW
LWO
DW
DW O
Analyte
1
2
1
2
1
2
1
2
------------------------------------------------------- Nitrate
205
121
160
4270
178
500
146
14 7
Nitrite
395
219
32
209
60
62
45
29
Ammonium
163
204
146
573
244
264
90
175 0
DIN
46600
93
1150
7600 13600
255
414
22 9
TPN
3250
173
99
151
329
155
224
12 6
DON
44
54
96
60
47
89
98
90
Phosphate
410
186
44 1560a
354
171
108
19 2
Oxygen
248
107
147
485
66
338
337
566a
a Anomalous variation can be attributed to a single outlie r
Table 5 : Analysis o.f Variance - P values are given if theOr- 7 -- '
are not significant, .but are nearly so .
Temperature was treated as a covariate .
.t
(** = P< .01, * = P<- .05)
Sti
'
ite 1
Site 2
A
----------------------------------------------- Analyte
Light Algae LxA Temp Light Algae LicA
Nitrate
**
0 .11
0 .0 6
---------------------------------------------------- -------------------------------
Ammonium
0 .09
**
DIN
Phosphate
Oxygen
--------- -
0 .07
*
0 .08
*
0 .05
*
t.
0.1
0 .14
0 .12
4 4
4
,
A'
7
e''
It is gratifying to find'that the ANOVA revealed significan t
relationships between light and oxygen fluxes in the chambers at bot h
sites . Given that even when flooded the sediment surface was well abov e
the compensation depth (the water depth at which net photosynthesi s
equals respiration, generally around 1% of surface light intensity) w e
would predict a net production of oxygen in the clear chambers and ne t
consumption of oxygen in the opaque chambers . That this indeed too k
place is revealed both in the net flux data and was clearly discerned b y
the ANOVA .
5 .2 .1 Temperature effect s
Between-site differences suggested by the ANOVA were also apparen t
in plots of inorganic nitrogen flux versus temperature (Figures 5A an d
5B) . DIN fluxes in DWO chambers increased linearly with temperature a t
Site 1 but exhibited a parabolic-like response to temperature at Site 2 .
Note that nitrate was always removed from the the overlying water a t
Site 1 and the net positive flux of DIN at that site was due to th e
opposing net positive flux of ammonium . The pattern at Site 2 wa s
significantly different : net release of DIN peaked around 13 °c, nea r
the mid-range of the temperatures encountered, and both nitrate an d
ammonium contributed to the net flux of DIN from the sediment community .
Between-site differences in the response of DIN fluxes to temperatur e
are also revealed when the data from all chamber treatments are combine d
(Figure 6) . The correlation between temperature and DIN flux i s
significant at Site 1 while no correlation is apparent at Site 2 .
Between-site differences were not as apparent in phosphate fluxe s
compared with the obvious differences found in fluxes of various DI N
forms . In spite of a number of outliers, the relationships betwee n
temperature, phosphate and oxygen fluxes in the DWO chambers (Figure 7 )
were among the strongest to emerge from the regression analyses .
The results of regressions of nutrient fluxes against temperatur e
are given in Table 6 . Differences between sites are again apparent . A t
Site 1, both DIN and nitrate fluxes correlated significantly wit h
temperature in most chamber treatments . This contrasts sharply with th e
results from Site 2, where the only significant correlations to emerg e
were between oxygen and temperature in the opaque chambers . When th e
data from both sites are combined, both oxygen and phosphate correlate d
with temperature in DWO chambers .
5:.2 .2 Summary
,mot
Results of the ANOVA, correlation, and regression analyses revealed '
surprising differences in the nutrient flux dynamics at our t'wo
NITROGEN FLUX VS TEMPERATUR E
Site 1
A.
30 0
200 -
100 -
C]
1
6
10
f
12
i
16
14
16
Temperature (degrees C )
B.
300
7
She 2
200 -
x
-100 -
-200
1
8
10
I
1
12
1
1
14
i
r
16
Temperature (degrees C)
Figure 5 : Sediment-water flux of nitrate _(Q), ammonium (-f-), an d
DIN (C), in dark chambers without macroalgae . Point s
indicate means f 1 S .E . Results of correlation analysi s
are presented in Table 5 .
18
DIN VS TEMPERATUR E
A
30 0
•
•
200 -
s
100 -
0
I
s
DIN Flux (umol m- 2 h' 1 )
-532 .4 + 40 .8 Temp .
0
8
r2
R
.4 3
10
16
18
16
18
Temperature (degrees C)
B
30 0
200 -
•
•
•
•
0
I
•
0
0
0
0
-300 8
10
12
14
Temperature (degrees C)
Figure 6 : Relationship between dissolved inorganic nitrogen flux an d
temperature at Site 1 (A) and Site 2 (B) for all treatments .
Points are means . Error bars have been omitted for clarity .
The regression line is drawn for Site 1 .
-29 -
P AND 0 VS TEMPERATUR E
Both sites
13
12 11-10-8 8
765 43J
2 :.r
1
•-
•
•
•
w
-2 -3
-4 -5 -+
-6 -7
-8
-9
8
+
1
10
1
k
12
l
r
14
r
+
r
16
i
18
Temperature (degrees C )
Figure 7 : Relationship between phosphate (II) and dissolved oxygen (+ )
fluxes and temperature with both sites combined . Data from
dark chambers without macroalgae . Points are means + 1 S .E .
Table 6 : Correlation matrix for Site 1 (A), Site 2 (B) ,
and both sites combined (C) . LW=clear chamber s
with algae LWO = clear chambers without alga e
DW = opaque chambers with algae
DWO=opaqu e
chambers without algae L = cle-ar chamb-e s
t
D= opaque chambers W=chambers with alga e
WO=chambers without algae All=all treatment s
Numbers in matrix refer to footnotes givin g
nearly significant correlation coefficients .
(** = P< .01, * = P< .05 )
A . Site 1
LW LWO
DW DW•O
L
D
W
WO Al l
-------------------------------------------------------0 vs Temp
1
2
P vs Temp
DIN vs Temp
4
*
5
**
Nitrate vs Temp
DIN vs 0
**
Nitrate vs 0
**
Ammonium v s 0
**
3
*
**
*
*
**
**
**
*
**
**
**
**
**
**
*
*
**
P vs 0
Nitrate v s P
Ammonium vs P
1
2
3
4
5
:
:
:
:
:
r*= .812
r*= .868
r*= .600
r*= .827
r*= .771
P .C.05= .87 8
P<.05= .87 8
P< .05= .66 6
P< .05= .87 8
P< .05= .878
B.
Site 2
LW LWO
DW DWO
L
D
W
WO Al l
-------------------------------------------------------- 0 vs Temp
Table 6 : continued
C . Both sites combine d
----------------------------------------- LW LWO
DW DWO
L
D
W
WO All ,
q vs Tem p
**
*
P vs Temp.
*
*
DIN vs Tem p
Nitrate vs Tem p
DIN" vs 0
**
**
Nitrate vs 0
1
2
**
Ammonium vs 0 * *
*
P vs 0
Nitrate vs P
Ammonium vs P
1:
2:
3:
4:
r*= :687
r*= .461
r*= .429
r*= .402
P< .95= .70 7
P< .05 = .46 8
P< .05= .46 8
P< .05= .44 4
-32-
3
intertidal study sites . Taking earlier reports of sediment-water flu x
dynamics in subtidal sediment communities (e .g . Nixon et al . 1976 ,
Boynton et al . 1980, Nixon 1981) as our model, we expected to fin d
relatively small between-site differences and generally stron g
correlations between sediment-water fluxes and temperature . We als o
predicted that the presence of macroalgae on the mudflats would alte r
the magnitude of sediment-water nutrient fluxes . This study reveal s
that tidal pulsing and the presence of autotrophic organisms in th e
sediment community introduce important additional sources of variabilit y
into the benthic system . The data collected during this study, althoug h
limited, seemingly argues against all three initial hypotheses . First ,
by nearly every yardstick applied, between-site differences outweig h
similarities. Second, the relationships between net sediment-wate r
fluxes and temperature (with the important exceptions of phosphate an d
oxygen) are generally weak or non-existent when the data from both site s
are combined . This may in part be remedied by a more extensive dat a
set . These initial results indicate that close coupling of temperature s
and sediment nutrient fluxes may be broken when benthic primar y
producers are introduced into the system . The relationship between ne t
sediment fluxes and these primary producers is clearly not straight forward : both the ANOVA and regression analyses failed to turn up ,
consistent relationships between the presence or absence of macroalga e
and net nutrient fluxes . However, the effect of the macroalgae o n
sediment nutrient dynamics becomes clearer when differences betwee n
treatments are analyzed (see Section 5 .4) .
5 .3
Nutrient Flux Stoichiometr y
Beginning with Redfield's pioneering work in the 1930's (se e
Redfield et al .
1963), ratios of changes in oxygen, nitrogen an d
phosphorus have been used to examine influences of the formation an d
decomposition of organic matter on water chemistry . The Redfield mode] .
predicts stoichiometric relationships between oxygen production an d
nutrient uptake during photosynthetic production of organic matter .
Similar stoichiometric relationships hold between the consumption o f
oxygen and nutrient remineralization during respiration . Since oxyge n
uptake or release can be converted into units of carbon produced o r
respired, the model provides a framework for examining the coupling o f
energy flow and nutrient cycling in aquatic systems .
Ratios of the net fluxes of oxygen and nutrients were calculate d
for various combinations of chamber treatments (Table 7) . Examples o f
the strongest relationships are shown in Figures 8A-8G . This analysi s
revealed one important pattern . The ratio of change in oxygen relativ e
to inorganic nitrogen (29-53) was at least double that predicted b y
Redfield's (16 :1) ratios . In other words, the sediment-water fluxes of
nitrogen on the mudflats were one half or less of what was expected
based on the level of metabolic activity occurring in the sediment . '
community . This result is surprisingly consistent with benthic flu x
studies from a variety of subtidal heterotrophic communities (Nixo n
(1981) .
However, the N/P ratio of fluxes in the other subtida l
sediments were generally low giving 0/P ratios consistent wit h
Redfield's predicted 212 :1 . In contrast, intertidal fluxes of 0/P-i n
Yaquina Bay, like those of 0/N, appear anomalously high . If th e
formation and decomposition of organic matter follows Redfield-lik e
stoichiometries, the high 0/P ratios of sediment fluxes indicates a sin k
of phosphorus, as well as nitrogen in the intertidal system . We are, _
however, left with the perplexing situation in which the overall NI P
flux is close to the expected value of 16 :1 .
These results point to fundamental similarities, as well as som e
differences, between nutrient dynamics in subtidal sediments and . our
results from intertidal communities . The net uptake of oxygen in ou r
dark chambers (1-3 mg-at 0 m-2 h -1 ) were within the range of sedimen t
oxygen demands reported for subtidal communities in Narrangans8tt .Ba y
(0 .31-4 .7 'mg-at m -2 h -1 , Nixon et al . 1976), Chesapeake Bay (2 .T-40 mgat m- 2 h- 1 , Boynton and Kemp 1985), and a shallow coastal pond in Rhod e
Island (0 .5-5 .9 mg-at m -2 h -1 , Nowicki and Nixon 1985a) . Total
metabolism in the mudflat community is therefore similar toy that foi-n d
in a variety of coastal marine sediment communities .
Seitzinger et al . (1980, 1985), Nixon (1981) and other' hav e
attributed the anomaly in 0/N ratio of benthic fluxes to the loss o f
fixed nitrogen in estuarine sediments by denitrification . Furthe r
evidence (Smith et al . 1985) suggests that denitrification rates in .
estuarine sediments are regulated by the nitrate "availability ."Given '
the abundance of nitrate in Yaquina Bay waters, this mechanism offers a
plausible explanation-for the high 0/N ratios found in our flu x
experiments . Other processes being equal, the loss of fixed .nitroge n
would also be expected to be revealed by benthic fluxes lows in nitrogen►
relative to phosphorus . Our intertidal fluxes apparently do not follo w
this pattern . The combination of diverse chemical, autotrophic an d
heterotrophic processes on the mudflats may obscure the cowling betwee n
nitrogen and phosphorus dynamics .
'
In summary, oxygen fluxes on the intertidal mudflats 100icat e
substantial levels of sediment metabolic activity . Denitrificatio n
probably accounts for a deficit in inorganic nitrogen relative to oxyge n
in sediment-water fluxes/Phosphate flux does not appear to be relate d
to nitrogen flux in any straightforward way, and the convergence of N/ P
fluxes near the Redfield ratio may be fortuitous . The high'ia.tio o f
oxygen to phosphorus fluxes also indicates that processes othe r; than th e
direct biological uptake and, remineralization of phosphorusimay b e
occurring on the mudflats .
k.
Table 7 : Ratios of elements calculated from flu x
measurements . Symbols and abbreviations as i n
Table 6 . Ratios were calculated for al l
significant plots and for the linear portions o f
plots that were not significant but showed str g
linearity .
Atkinson &
Analytes Signif . Treatment Site Ratio Redfield Smith(1984 )
DIN vs 0
**
**
t*
**
*
**
**
All
L
LW
WO
L
LWO
LW
both
150
both
53
both
38
1
37
1
35
1
29
1
36
Nitrate vs- 0 N .S .
N .S .
*
*
**
**
L
both
11 0
LW
both
75
W
1
10 0
WO
1
68
L
1
66
LW
1
66
Ammonium vs 0 **
**
*
**
**
**
*
L
both
11 0
LW
both
67
WO
1
85
L
1
76
LWO
1
57
LW
1
81
D
2
82
P vs 0
WO
DW O
DW O
WO
both
2500
both 120 0
1
82 0
2 110 0
DW O
WO
L
LW
L
1
2
2
2
both
DIN vs P
N .S .
*
N .S .
N .S .
N .S
N .S
N .S
N .S
Nitrate vs P N .S
.
.
.
.
.
-35-
28
10
14
29
6
17
18
J
:r
211
55 0
' i$
)3 0
DIN VS OXYGE N
A . Site 1, clear chambers
30 0
^
.c
o
20 0
B
100
0
0
a
C
CI
C
-8
T
-4
-I
0
T
4
8
q Flux (mg-at m-2
B.
300
•
200
•
100
12
h-i )
DIN VS OXYGEN
Site 1, chambers without alga e
n
a
a
0
a
a
-100-•
a
a
-200 - j
-300
f
-6
i
-4
i
I
F
-2
Z
0
q flux (mg-at m-2
r
I
2
a
4
6
)
Figure 8 : Examples of element relationships derived from fluxes unde r
various conditions . Points are means . Error bars hav e
been omitted .
NITRATE AND AMMONIUM VS 0
C. Site 1, chambers without alga e
200
+
+
150
0.
6
t
N-
+
100
Z
.►+
a
+
+
50
+
I
E
Nitrat e
+ Ammonium
0 T
Y
+
a
n
p
u
-50
+
T
ci
Q
+
c
X
a
-100
z
-15 0
n
R
-200
n
-250
-4
-- 6
-2
0
4
2
6
0 Flux (mg-at m-2_ h-1 )
AMMONIUM VS OXYGE N
D. Both sites, clear chambers
250
200
150
c
n
100
50
n
a
t
0
Z
c
c
Q
-50
-100
-8
Q
s
s
-4
q
s
0 Flux (mg-at m- 2
Figure 8 : continue d
-37 -
8
4
h
)
-
12
AMMONIUM VS OXYGE N
E. Site 1, clear chambers
220
200
a
180
160
14 0
r
120
n
10 0
80
60
•
•
•
40
20
0
-20
- 40
Q
-60
- 80
t
-100
I
-8
i
{
-4
{
F
I
I
4
q
0 Flux (mg-at m- 2
{
8
1
12
h-1 )
AMMONIUM VS OXYGE N
F.Both sites, clear chambers with algae
250
200
a
150
a
e
Z
-5 0
-100
-8
{
1
-4
0
i
F
0 Flux (mg-at m- 2
rigure 8 : continued
-38 -
{
4
{
8
h- 1 )
{
F
12
PHOSPHATE VS OXYGE N
G . Both sites . dark chambers without alga e
n
0
0
0
-7
Figure 8 : continue d
1
-5
--
0
1
i
i
-3
-1
0 Flux (mg-at m-2 h-1 )
5
r
7
5 . 14 Influence of Macfoalgae on Intertidal Nil .
T.
We were unable to discern any direct rre'llitil'MI'Apis''tiOt!
flux of oxygen and nutrients and the presence or absence of r erO1pe
in the flux chambers (Tables 5 and 6) . However, our experimental desig n
allowed us to compare the fluxes in chambers containing algae to thos e
without algae . The difference between these treatments therefore can b e
taken to represent a measure of the contribution of macroalgae to fluxe s
occurring in the chambers . This, of course, assumes that th e
differences between treatments are in fact due to the algae and not t o
other sources of within-site variability . This is admittedly a shak y
assumption . Use of duplicate chambers did however provide an estimat e
of within-treatment variability .
Differences between the fluxes of the various forms of DIN in clea r
chambers with and without macroalgae (LW minus LWO) are Shown plotte d
against temperature at Sites :,1 and 2 in Figure 9 . These figures onc e
again indicate significant between-site differences in the balanc e
between the net nitrogen uptake and remineralization . At Site 1, ne t
remineralization of nitrogen appears to exceed the uptake capacity o f
the macroalgae at temperatures above about 13 C (Figure 9A) . At Site 2 ,
regardless of the temperature, the differences between fluxes in the L W ,
and LWO chambers was always negative (Figure 9B) . This implies tha t
macroalgal uptake of nitrogen (especially nitrate) was greater t hran_th e
total flux of remineralized nitrogen from the sediment . The differc e
between sites does not appear related simply to differences i n
macroalgal abundance at the two sites, but rather to greater net fluxo f
remineralized nitrogen at Site 1 . Examination of macroalgal influence s
on phosphate and oxygen fluxes revealed no consistent trends or
J.
differences between sites .
Oxygen and nutrient flux dynamics on the intertidal mudflats ar e
clearly complex . Our ability to clearly discern the effects o f
macroalgae on these processes may be obscured by within- and betwee n
site variability . Nevertheless, as shown in Table 8 there appeared
to be an inverse relationship between the effect of macroalgae on DI N
and oxygen fluxes in the clear chambers . This finding implies that th e
net uptake of DIN took place when the intertidal sediment community ,
taken as a whole, was autotrophic (i .e ., net macroalgal productio n
exceeded sediment oxygen demand) . Likewise, net release of DI N
proceeded only when the community was heterotrophic (net macroalga l
production was less than sediment oxygen demand) . Curiously, our tw o
sites seem to separate along these lines . Oxygen fluxes at Site 2 wer e
always positive in the LW chambers while at Site 1 net oxygen fluxes i n
the LW chambers were generally negative . We take 'this as evidenc e
supporting our initial hypothesis that macroalgal nutrient deman d
modifies the magnitude of sediment-water nutrient fluxes .
NET MACROALGAL INFLUENCE VS TEM P
•
14 0
120-100 80-i
60- 40 20 0
-20
-40
-6 0
-8 0
-10 0
-120
+
0
+
0
d
8
10
14
12
16
18
16
18
Temperature (degrees C
^ 40
B
+
4.
0
3
•
u
C
•
-8 0
-100 -120 -140-160--180 ,
`v
-200 -~
x
3
E
O
a
+
+
0
i
0
a
-I
10
0
12
14
Temperature _(degrees C)
Figure 9 : Comparisons of net influence of macroalgae on inorgani c
nitrogen fluxes (C =nitrate, + =ammonium, =DIN) : [mea n
flux from light chambers with algae] minus [mean flux fro m
light chambers without algae] . At site 1 (A) and site 2 (B) .
Points are means with error bars omitted .
-41-
Table 8 .
Matrix showing the inverse relationship between intertida l
community metabolism (A02) and the effect of sediment-associate d
macroalgae on sediment-water exchanges of dissolved inorganic nitroge n
(A DIN) . Plus sign (+) indicates net flux into water, minus sign (- )
indicates net flux from water . Sign in parentheses indicate near-zer o
flux . Data from clear (LW and LWO) treatments .
Site 2
Site 1
Date
~DIN a
°02
9- 9-84
b
'ADIN
02
-
+
-
+
1-13-85
(-)
+
3- 8-85
-
+
+
-
9-22-84
10- 6-84
+
-
(+)
(+ )
10- 7-84
12- 4-84
+
(- )
4-19-85
-
+
6-30-85
-
+
7- 1-85
a A DIN = Net DIN flux in LW chambers minus net DIN flux in LWO chamber s
b A 0 2 = net oxygen change in LW chambers
5 .5 Nutrient Removal Capacity of Intertidal Macroalga e
Our initial objective in this study was to assess the role o f
intertidal sediment communities in nutrient cycling processes in th e
Yaquina River Estuary . In particular, we were interested in determinin g
whether the growth of intertidal macroalgae could exert a significan t
influence on the amount of inorganic nutrients introduced into th e
estuary via the flow of the Yaquina River . To make this assessment w e
compared the amounts of inorganic nitrogen and phosphorus entering th e
estuary via riverflow with estimates of macroalgal nutrient demand an d
net sediment nutrient remineralization determined at our study sites .
Estimates of daily inputs of nitrate and phosphate were calculate d
as the product of the concentration of inorganic nutrients (in moles pe r
liter) in river water and the flow of the Yaquina River (in liters pe r
day) into the estuary . Nutrient concentrations in the river where i t
enters the estuary were determined at monthly or bi-monthly interval s
from July 1983 to June 1984 (Garber et al ., unpub . data) . Riverflow o f
the Yaquina River was taken from the ten-year averaged data of the USG S
gauging station at Chitwood (Friday and Miller 1984) . The amount o f
nutrients entering estuarine waters from sediment remineralization wa s
calculated by assuming that the net positive fluxes from our study site s
were representative of both intertidal and subtidal estuarine sediments .
Total daily nutrient loadings, which we termed "supply", were taken t o
be the sum of river input and bay-wide sediment remineralization .
Daily rates of nutrient removal by the macroalgae associated wit h
intertidal sediments was estimated from nutrient uptake data ,
photoperiod, and estimates of bay-wide macroalgal biomass and coverage .
Macroalgal nutrient uptake (moles per gdw per hour) had been determine d
by incubating samples of macroalgae in clear and dark bottles of ba y
water under in situ conditions during each chamber deployment . Hourl y
uptake rates were then multiplied by the number of daylight hours on th e
day of incubation (see photoperiod data in Figure 2B) . Davis' s
estimates of Enteromorpha biomass (Figure 3A) and coverage were taken t o
be representative of bay-wide macroalgal abundance .
These calculations (Figure 10 and Appendix 3) indicate that th e
uptake of nitrate by intertidal macroalgae can indeed be a significan t
sink of inorganic nitrogen and phosphorus during the summer and fall .
Our results suggest that during their growth season (June-October) ,
nutrient demand by the macroalgae could remove from 40% to 58 times th e
amount of nitrate, and from 23% to 218 times the amount of phosphat e
supplied to the estuary via riverflow and sediment remineralization . I t
should be noted, however, that the period of peak macroalgal abundanc e
(summer and fall) is out of phase with the period of maximum riverin e
nitrate input (winter and spring) . On the other hand, the supply o f
phosphate to estuarine waters appears to be driven primarily by the flux
of remineralized phosphate from the sediments which, as we note d
earlier, is a temperature-dependent process . Phosphate supply an d
demand therefore appear to. be in phase throughout the year .
Unfortunately, our data do not allow a more tightly-constrained annua l
budget . For this we need better estimates of riverine and othe r
nutrient inputs, more comprehensive measurements of both siubtidal an d
intertidal sediment-water fluxes, and better surveys of macroa
l
biomass and coverage . Nonetheless, our calculations clearly point
toward the importance of macroalgae and intertidal sediment-water ,
exchanges as terms that ought to be included in the nutrient balm- 00
sheet of the Yaquinia' Estuary .
_I'+
1
' •,
S
L
J
r'
,
4'
11
150 --
REMOVAL COMPARED TO SUPPLY
140 -
20 0
Nitrate
T
130 ^ 120 -
-v
110 -
q
0
ET
100 -
2'
n.r,
80 -
3a
ul =
ov
©
N
Remova l
Su p ply
90 -
70 60 -
0
50 -
•
E
•
40 30 -
5
B
14
Phosphate
P Remova l
P
Supply
0
6
2
7
8
9
Month
Figure 10 : River supply of nitrate (A) and phosphate (B) compared t o
calculated macroalgal removal capacity . Data used fo r
Figures are given in Appendix 3 .
-45 -
.
4
•
6.
CONCLUSIONS
I
'-
r
1
.
1
,Tr
I -
.J
Seasonal patterns of sediment community metabolism and ne t
sediment-water nutrient fluxes were investigated at two intertidal site s
on the south shore of the Yaquina River Estuary in Oregon . Ne t
sediment-water exchanges of oxygen, nitrate, nitrite, ammonium ,
dissolved organic nitrogen, and phosphate were determined using in sit u
"bell jar" metabolic chambers . A fully crossed two-by-two experimenta l
design was employed to examine the influences of light and the presenc e
of sediment-associated macroalgae on community metabolism and nutrien t
exchanges . Chambers were deployed at each site five times during th e
period from September 1984 to July 1985 .
The intertidal estuarine environment is characterized by extrem e
variability introduced by complex interactions of tides, photoperiod ,
and seasonal climate . It was therefore not surprising to fin d
considerable within-site and between-site variations in communit y
metabolism and nutrient exchanges . Total sediment community metabolism ,
measured as changes in oxygen concentrations in the metabolic chambers ,
ranged from -10 to 49 mg-at 0 m- 2 h -1 . These rates of sedimen t
metabolism fall well within the range reported for other coasta l
systems . Greatest variability in oxygen fluxes occurred in chamber s
that contained macroalgae . Net fluxes of DIN (nitrate + nitrite +
ammonium) ranged from -380 to 270 ug-at N m -2 h -1 , and exhibited th e
greatest within-site variability . This was particularly evident i n
chambers containing macroalgae . Coefficients of variation in DIN fluxe s
in chambers containing macroalgae ranged from 93% to 466 times the mea n
flux at Sites 2 and 1, respectively . Phosphate fluxes ranged from -1 5
to 54 14g-at p m -2 h -1 , and appeared less variable, especially in dar k
chambers (C .V ., 100-200%) . This suggests more uniformity in sediment associated phosphorus remineralization at the intertidal sites . Ne t
fluxes of DON exhibited the least within-site and between sit e
variability, giving C .V.'s for each site that ranged from 44-98% .
jl
A.
The carbon :nitrogen ratio of intertidal macroalgae at our stud y
sites ranged from seasonal lows of about 6-7 in mid-winter, to highs o f
8-10 in fall, perhaps reflecting changes in the concentration o f
inorganic nitrogen in Yaquina Bay waters . At no time, however, did th e
C :N ratio of the macroalgae indicate nitrogen-limited growth conditions .
As expected, net fluxes of oxygen were strongly correlated wit h
light at both sites . Fluxes of nutrients, however, exhibite d
significant between-site differences . Both nitrate and DIN fluxes a t
Site 1 showed significant correlations with temperature and oxyge n
fluxes, particularly in the light . We were unable to detect simila r
correlations at Site 2 . Fluxes at Site 1 appeared to be dominated b y
temperature-sensitive processes . Macroalgal influences at this sit e
appeared minimal . Analysis of variance of the sediment flux data
I
- 47_
i f
indicated light and algae, rather than temperature, contributed more t o
variations in the fluxes of nitrate, DIN and oxygen at Site 2 . Althoug h
we lack convincing biomass data to support the point, macroalgal biomas s
appeared greater at Site 2 than at Site 1 .
Fluxes of nitrogen and phosphorus, relative to oxygen, sugges t
sinks of both these elements in the intertidal community . Fluxes o f
inorganic nitrogen were one-half or less of what would be expected a t
the measured rates of oxygen fluxes . Loss of nitrogen via microbia l
denitrification appears to be the most likely mechanism for the loss o f
fixed nitrogen from the intertidal sediment-water system . The mechanis m
producing high O :P ratios in the sediment-water fluxes is not known .
Whatever the mechanism, the apparent losses of both nitrogen an d
phosphorus resulted in net changes of these elements close to th e
predicted ratios of 16 :1 .
Comparisons of nutrient sources and sinks in the Yaquina Rive r
Estuary indicate that intertidal macroalgae can be a significant sink o f
inorganic nitrogen and phosphorus during the summer and fall . Ou r
results suggest that during their growth season (June-October) ,
macroalgae could remove from 40% to 58 times the amount of nitrate, an d
from 23% to 218 times the amount of phosphate supplied to the estuar y
via riverflow ' and sediment remineralization . We note, however, that th e
period of peak macroalgal abundance (summer and fall) is out of phas e
with period of maximum riverine nitrate input (winter and spring) . Th e
supply of phosphate to estuarine waters appears to be driven primaril y
by the temperature-dependent flux of remineralized phosphate from bot h
intertidal and subtidal sediments . Phosphate supply and deman d
therefore appear to be in phase throughout the year .
Better estimates of natural and anthropogenic nutrient inputs ,
subtidal and intertidal sediment-water fluxes, and macroalgal biomas s
and coverage are needed to construct a more tightly-constrained nutrien t
budget for the Yaquina Estuary . Nonetheless, our calculations clearl y
point toward the importance of macroalgae and intertidal sediment-wate r
exchanges as terms to be included in the nutrient balance sheet of th e
Yaquina Estuary .
.
1
7,
LITERATURE CITL D
Atkinson, M .J : and S .U. Smith .
1983 . C :N :P : ratios of beent1Ybic ,in e
.
28
plants . Limnol . Oceanogr
:5'68-574 .
.1
Boynton, W .R . and W .M . Kemp .
Nutrient regeneration and oxyge n
1985 .
consumption by sediments along an estuarine salinity gradient . Mar .
Ecol . Prog . Ser . 23 : 145-55 .
Boynton, W .R ., W .M . Kemp, and C .G . Osborne ., 1980 . Nutrient file
s
across the sediment-water interface in the turbid zome- o& .a 4oe 11 ,
plain estuary . p . 93-109 . In V .S . Kennedy (ed .) . Estuarine .
Perspectives . Academic Press, New York .
F.
-
1 ,
Brown, G .W ., A .R . Gahler, and R .B . Marston . 1973 . Nutrient losse s
after clear-cut logging and slash burning in'the oregon coast range .
Wat . Resources Res . 9 :1450-1453 .
Burt, W .V.
1956 .
Flushing of pollutants in the Yaquina River Estuary .
Office of Naval Research Contract #1286(02) .
Oregon State College
School of Science Technical Report 56-1 .
Burt, W .V . and W .B . McAlister .
Recent studies in the hydrography
1959 .
of Oregon Estuaries . Fish Commission of Oregon . Research Brief s
7(1) :14-27 .
Chubb, C .J . and J .H . Stoner . Water quality investigations in th e
Loughor Estuary and Burry Inlet .
p . 1 :2/1-4 :2-9.
In A. Nelson-Smit h
and E.M . Bridges (eds .) . Problems of a small estuary . Quadrant Press ,
Ltd . Swansea .
Conover, J .T .
Seasonal growth of benthic marine plants a s
1958 .
related to environmental factors in an estuary . Pub . Inst . Mar . Sol .
5 :97-147 .
Davis, M .W .
1981 .
Production dynamics of sediment-associated algae i n
two Oregon estuaries . Ph .D . Dissertation . Oregon State University .
Corvallis .
135 p .
Davis, N.W . and C .D . McIntire .
1983 .
Effects of physical gradients o n
the production dynamics of sediment-associated algae . Mar . Ecol . Prog .
Ser . 13 :103-11 11.
D'Elia, C .F ., P .A . Steudler, and N . Corwin . 1977 . Determination o f
total nitrogen in aqueous samples using persulfate digestion . Limnol .
Oceanogr . 22 :760-7611 .
L.
- 49 -
Fitzgerald, W .J ., Jr . 1978. Environmental parameters influencing th e
growth of Enteromorpha clathrata (Roth) J. Ag . in the intertidal zone o f
Guam . Bot . Mar . 21 :207-220 .
Friday, J . and S .J . Miller . 1984 . Statistical summaries of streamflo w
data in Oregon . Vol . 2 . Western Oregon . U .S .G .S . Open-file Rept . 84 454 . Portland, Oregon .
Golterman, H .L ., R .S . Clymo, M .A .M . Ohnstad . 1978 . Methods fo r
physical and chemical analysis of fresh waters . 2nd edition . IBP
Handbook No . 8 . Blackwell Scientific Publications . Oxford . 213 p .
Hanisak, M .D . 1983 . The nitrogen relationships of marine macroalgae .
p . 699-730 . In E .J . Carpenter and D .G . Capone (eds .) Nitrogen in th e
marine environment . Academic Press, New York .
Jaworski, N.A . 1981 . Sources of nutrients and the scale o f
eutrophication problems in estuaries . p . 83-110.
In B .J . Neilson an d
L .E . Cronin (eds .) Estuaries and nutrients . Humana Press . Clifton, NJ .
Karentz, D . and C .D . McIntire . 1977 . Distribution of diatoms in th e
plankton of Yaquina Estuary, Oregon . J . Phycol . 13 :379-388 .
Kaul, L .W . and P.N . Froelich, Jr . 1984 . Modeling estuarine nutrien t
geochemistry in a simple pristine system . Geochim . Cosmochim . Acta .
Kautsky, L . 1982 . Primary production and uptake kinetics of ammoniu m
and phosphate by Enteromorpha compressa in an ammonium sulfate industry
outlet area . Aquatic Bot . 12 :23-40 .
Kemp, W .M ., R .L .Wetzel, W .R . Boynton, C .F . D'Elia, and J .C . Stevenson .
1982 . Nitrogen cycling and estuarine interfaces : some current concept s
and research directions . p . 209-230 .
In V .S . Kennedy (ed .) . Estuarin e
Comparisons . Academic Press, New York .
Kennedy, V .S . (ed .) . 1984 . The estuary as a filter . Academic Press ,
Orlando . 511 p .
Kentula, M .E . 1983 . Production dynamics of a Zostera marina L . bed i n
Netarts Bay, Oregon. Ph .D . Dissertation . Oregon State University ,
Corvallis .
158 p .
Klump, J .U . and C .S . Martins . 1981 . Biogeochemical cycling in a n
organic rich coastal marine basin : 2 . nutrient sediment-water exchang e
processes . Geochim . Cosmochim . Acta 45 :101-122 .
In C .S. Lobban an d
Kremer, B .P .
1981 . Carbon metabolism .
p . 492-533 .
M .J . Wynne (eds .) . Biology of Seaweeds . Biol . Monogr . 17 . Univ .
Calif . Press, Berkeley .
Kulm, L .P .
1965 .
Sediments of Yaquina Bay, Oregon . Ph .D .
Dissertation . Oregon State University . Corvallis .
MacKay, D .W . and T.M . Leatherland .
1976 . Chemical processes in a n
estuary receiving major inputs of industrial and domestic wastes . p .
185-218 . In J .D . Burton and P .S . Liss (eds .) . Estuarine Chemistry .
Academic Press, New York .
List, R .J .
1971 . Smithsonian meteorological tables . Smithsonia n
Smithsonian Inst . Press .
Miscellaneous Collections . Vol 114 .
Washington, DC .
Malone, T .C .
1984 .
Anthropogenic nitrogen loading and assimilatio n
In
capacity of the Hudson River Estuarine system, USA . p . 291-311 .
V.S . Kennedy (ed .) . The Estuary as a Filter . Academic Press, Orlando .
Mann, K.H .
1973 .
growth . Science
Seaweeds : their productivity and strategy fo r
182 :975-981 .
Maybeck, M .
1982 . Carbon, nitrogen and phosphorus transport by worl d
rivers . Am J . Sci . 282 :401-450 .
McCaffrey, R .J ., A .C . Meyers, E . Davey, G . Morrison, M . Bender, N .
Ludke, D . Cullen, P . Froelich, and G . Klinkhammer .
1980 .
The relation
between pore water chemistry and benthic fluxes of nutrients an d
manganese in Narragansett Bay, Rhode Island . Limnol . Oceanogr . 25 :996 1011 .
McComb, A .J ., R .P . Atkins, P .B . Birch, D .M . Gordon, and R .J . Lukatelick .
1981 . Eutrophication in the Peel-Harvey estuarine system, Wester n
Australia . p . 323-342 . In B .J . Neilson and L .E . Cronin (eds .) .
Estuaries and Nutrients . Humana Press . Clifton, New Jersey .
Mortimer, C .H.
1941 .
The exchange of dissolved substances between mu d
and water in lakes (Parts I and II) . J . Ecol . 29 :280-329 .
Miller, J .H.
1974 .
Nutrient losses and nitrogen mineralization o n
forested watersheds in Oregon's coast range . Ph .D . Dissertation .
Oregon State University . Corvallis .
Nixon, S .W .
1981 .
Remineralization and nutrient cycling in coasta l
marine ecosystems . p . 111-138 . In B .J . Neilson and L .E . Cronin (eds .) .
Estuaries and Nutrients . Humana Press . Clifton, New Jersey .
Nixon, S .W ., C .A . Oviatt, and S .S . Hale . 1976 . Nitrogen regeneratio n
and the metabolism of coastal marine bottom communities . p . 269-283 .
In J .M . Anderson and A . Macfadyen (eds .) . The role of terrestrial an d
aquatic organisms in decomposition processes . Blackwell Scientifi c
Publications . Oxford .
Nixon, S .W . and M .E .Q. Pilson . 1984 . Nitrogen in estuarine and coasta l
marine ecosystems . p . 565-648. In E.J . Carpenter and D .G . Capon e
(eds .), Nitrogen in the marine environment . Academic Press, NY .
Nowicki, B .L . and S .W . Nixon . 1985a . Benthic 'community metabolism in a
coastal lagoon ecosystem . Mar . Ecol . Prog . Ser . 22 :21-30 .
Nowicki, B.L . and S .W . Nixon . 1985b . Benthic nutrient remineralizatio n
in a coastal lagoon ecosystem . Estuaries 8 :182-190 .
Odum, E .P . 1971 . Fundamentals of ecology . 3rd . ed . W .B . Saunders .
Philadelphia. 574 p .
Officer, C .B ., D .R . Lynch, W .M . Kemp, and W .R . Boynton . 1985 .
Estimation of benthic respiration parameters from field data . Est .
Coast . Shelf Sci . 21 :357-364 .
Okuda, T . 1960 . Metabolic circulation of phosphorus and nitrogen i n
Matsushima Bay (Japan) with special reference to the exchange of thes e
elements between sea water and sediments . Trabalhos do Instituto d e
Biologia Maritima e Oceanografia (Recife) . Vol . II(1) :7-154 .
Oregon Division of State Lands . 1973 . Oregon estuaries . State o f
Oregon State Land Board, W .S . Cox, Director .
Owens, N .P .J . and W .D .P . Stewart . 1983 .
Enteromorpha and the cyclin g
of nitrogen in a small estuary . Est . Coast . Shelf Sci . 17 :287-296 .
Pregnall, A .M . 1983 . Release of dissolved organic carbon from th e
estuarine intertidal macroalgal Enteromorpha prolifera .
Mar . Biol .
.
73 :37-42
Redfield . A .C ., B .H . Ketchum, and F .A . Richards . 1963 . The influenc e
of organisms on the composition of sea water . p . ' 26-77.
In M .N . Hil l
(ed .) . The Sea . Vol 2 . Interscience .
Ryther, J .H. 1959 . Potential productivity of the sea . Scienc e
130 :602-608 .
Ryther, J .H . and W .M . Dunstan . 1971 . Nitrogen, phosphorus, an d
eutrophication in the coastal marine environment . Science 171 :1008 1013 .
Ryther, J .H . and C .B . Officer . 1981 . Impact of nutrient enrichment o n
water uses . p . 247-261 . In B .J . Neilson and L .E . Cronin (eds .) . Estuar•
ries and nutrients . Humana Press . Clifton, NJ .
Sawyer, C .N . 1966 . The sea lettuce problem
Poll . Contr . Fed . 37 :1122-1133 .
in Boston Harbor . J . Wat .
Schemel, L .E ., D .D . Harmon, S .W . Hager, D .H . Peterson . 1984 . Respons e
of northern San Francisco Bay to riverine inputs of dissolved inorgani c
carbon, silicon, nitrogen, and phosphorus . p . 221-240 .
In V .S . Kenned y
(ed .) . The estuary as a filter . Academic Press . Orlando .
Schindler, D .W . 1981 . Studies of eutrophication in lakes and thei r
relevance to the estuarine environment . p . 71-82 .
In B .J . Neilson and
L .E . Cronin (eds .) . Estuaries and nutrients . Humana Press, Clifton ,
NJ .
.1
Schindler, D .W . and E .J . Fee . 1973 . Diurnal variation of dissolve d
inorganic carbon and its use in estimating primary production and C0 2
invasion in lake 227 . J . Fish . Bd . Can . 30 :1501-1510 .
Seitzinger, S .P . and S.W . Nixon . 1985 . Eutrophication and the rate o f
denitrification and N 2 0 production in coastal marine sediments . Limnol . ,
Oceanogr . 30 :1332-1339 .
Seitzinger, S .P ., S .W . Nixon, M .E .Q . Pilson, and S . Burke . 1980 .
Denitrification and N2O production in near-shore marine sediment .
Geochim . Cosmochim . Acta 1853-1860 .
-
.
Sharp, J .H ., J .R . Pennock, T . M . Church, J .M . Tramontano, and L .A .
Cifuentes . 1984 . The estuarine interaction of nutrients, organics, an d
metals : a case study in the Delaware Estuary . p . 241-258 .
In V .S .
Kennedy (ed .) . The estuary as a filter . Academic Press, Orlando .
Shellem, B .H. and M .N . Josselyn . 1982 . Physiological ecology o f
Enteromorpha clathrata (Roth) Grev . on a salt marsh mudflat . Bot . Mar .
25 :541-549 .
Simonstad, C .A. and R .C . Wismar . 1983 . Variability in estuarine foo d
webs and production supporting juvenile salmon (Oncorhynchus) .
Draft o f
paper presented at Workshop on Influence of Ocean Conditions on th e
Production of Salmonids . Newport, OR .
Smayda, T .J . 1974 . Bioassay of the growth potential of the surface o f
lower Narragansett Bay over an annual cycle using the diato m
Thallassiosira pseudonana (oceanic clone, 13-1) . Limnol . Oceanogr .
19 :889-901 .
r-
53-
:`
~ ."
-
.
r
Smith, S .V. 1981 . Marine macrophytes as a global carbon sink . Scien e
211 :838-840 .
Solorzano, L . 1969 . Determination of ammonia in natural waters' by the
phenolhypochlorte method . Limnol . Oceanogr . 14 :799-b01 .
Strickland, J .D .H . and T .R. Parsons . 1972 .
A practical handbook elf
seawater analysis . 2nd ed . Fish . Res . Bd . Canada Bull . 167 . O t-taw:a=: :310 p .
Thom, R .M . 198 14 . Composition, habi=tats, seasonal changes an d
productivity of mac rroalgae in Grays Harbor Estuary, Washington .
Estuaries 7 :51-60 .
U .S . EPA. 1982 . Chesapeake Bay Program technical studies :
a
synthesis . U .S. EPA, Chesapeake Bay Program . Annapolis, Maryland .
Walsh, J .J ., G .T . Rowe, R .L . Iverson, and C .P . McRoy . 1981 . Biologica l
export of shelf carbon is a sink of the global C0 2 cycle . Natur e
291 :196-201 .
Welsh, B.L . 1980 . Comparative nutrient dynamics of a marsh-mudfla t
ecosystem . Est . Coast . Mar . Sci . 10 :143-164 .
Zeitzschel, B . 1980 . Sediment-water interactions in nutrient dynamics .
p . 1 95-218 . In K .R . Tenore and B .C . Coull (eds .) . Marine benthi c
dynamics . University of South Carolina Press . Columbia, SC .
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Appendix 2 : Mean sediment-water fluxes calculated from duplicate treatments during each chambe r
deployment . All units are micromoles per square meter per hour except oxygen which i s
milligram-atoms per square meter per hour . Abbreviations are as in text . Nitrit e
fluxes were not measured for the first two deployments, and TPN and DON fluxes wer e
not determined for the last two deployments .
------------------------------------------------------------------------------------------------ Cruis e
Date
Site Treatment Nitrat e
Nitrite
Ammonium
DIN
TPN
DON
Phosphate
Oxyge n
9-9-84
2
LW
LWO
DW
DWO
9-22-84
1
LW
LWO
DW
DWO
10-6-84
1
LW
LWO
9 .968209
33 .24003
18 .59206
-22 .7814
0
0
0
0
212 .7735
183 .6116
175 .8498
124 .8684
657 .5889 855 .7609
90 .34309 153 .1679
-76 .9639 41 .15638
42 .81941
98 .5141
222 .7417 1322 .628
1150 .19
216 .8516 -383 .68 -1570 .2
194 .4419 2096 .288 1901 .846
102 .0869 2601 .083 2498 .996
8 .264468 31 .3887 5
8 .128802 -4 .1919 2
16 .31783 -10 .015 8
11 .81032 -8 .416 6
-5 .57973
3 .615009
-8 .38778
-2 .71604
-7 .9985
-5 .0127
-9 .5115
-2 .8305
5
4
6
2
-0 .30310 -14 .8409
-26 .796 168 .1798
-0 .62945 -4 .61391 -46 .3571 -278 .062
-0 .10573 1 .900193 -41 .9213 131 .8237
0 .838611 38 .83638 31 .51292 -244 .303
194 .9758
-224 .746
76 .55179
-275 .816
12 .40657
7 .498301
-9 .2861
8 .672791
5 .41224 2
6 .16151 9
-5 .4075 2
-5 .7026 7
DWO
-73 .049
-8 .47447
7 .230287
34 .14123
-9
-3
-4
-0
-261 .749
-166 .353
-493 .435
-442 .779
-14 .6061
4 .246959
40 .56054
53 .65632
49 .1605 7
8 .91083 6
-1 .4397 5
-3 .0142 5
-3 .22324
112 .348 -81 .3715
-13 .3848 74 .04677 -122 .018
-3 .03002 -39 .2059 -172 .132
3 .223244
50 .9454 -114 .81
DWO
2
0 -141 .111 -198 .172
0 -46 .7084 -62 .8248
0 -107 .02
-118 .12
0 -50 .0416 -55 .6947
-11 .652
-39 .3076
-43 .7158
-8 .16207
DW
10-7-84
-57 .0609
-16 .1164
-11 .2006
-5 .65307
LW
LWO
DW
.03129 -121 .547 -203 .627
.83053 1 .715149 -10 .5899
.62495 -1 .11896
1 .48638
.21796 77 .62851 111 .5518
-465 .376
-176 .943
-491 .949
-331 .227
12-4-84
1
LW
LWO
DW
DWO
-190 .496
-182 .68
-129 .896
-168 .979
1-13-85
2
LW
LWO
-4 .03214 -1 .38766 -17 .9581
11 .19574 1 .074523 -15 .0716
12 .26346 -5 .67292 -94 .3737
-20 .0361 -7 .62821 -56 .3715
-23 .3779
-2 .80131
-87 .7831
-84 .0358
198 .1004 221 .4783
-2 .12188
242 .0712 244 .8725 -4 .18635
1855 .281 1943 .064 -1 .01785
2168 .971 2253 .007 0 .0820757
7 .26958 3
7 .30259 4
7 .04489 8
7 .64752 3
DWO
-24 .4024 1 .046995
47 .2137
137 .1811 6 .240749 14 .31992
-97 .4447 -15 .7297 -48 .9285
90 .10752 -18 .9036 9 .645544
23 .85829
157 .7417
-162 .103
80 .84944
683 .3497 659 .4914
-2 .59688
449 .6307
291 .889
2 .019793
1138 .421 1300 .524 -0 .189613
1259 .609
1178 .76 -0 .189613
4 .45096 5
1 .96950 5
3 .72219 1
1 .61583 5
DW
DWO
3-8-85
2
LW
LWO
DW
17 .65319 99 .02472 0 .7816585 8 .74886 7
-240 .294 -118 .276
7 .034927 1 .87027 2
-832 .335 -660 .203
3 .126634
-0 .040 4
-136 .658 -21 .8484
2 .866081 -0 .2227 8
4-19-85
1
LW
LWO
DW
DWO
-286 .377
-3 .6578
-89 .28 -379 .315 -1390 .11
-1010 .8
-224 .327 -5 .67634 -47 .2314 -277 .235 -1885 .29 -1608 .06
-94 .1581 -11 .5042 -60 .5037 -166 .166 -79 .7005 86 .46543
-33 .3624 -12 .1639 -2 .21116 -47 .7374 -89 .235 -41 .4976
-6 .16579 13 .8880 2
2 .206087 6 .60924 7
-3 .20744 -5 .4608 1
5 .549933 -2 .6207 5
6-30-85
2
LW
LWO
-257 .144
-113 .287
37 .26291
183 .147
0 .580097
3 .438879
2 .623074
3 .236252
24 .46575 -232 .098
21 .53933 -88 .0086
95 .25901
135 .145
35 .47056 221 .8538
0
0
0
0
0
0
0
0
-15 .3203
-12 .8837
-2 .03454
-3 .55337
3 .17355 8
-4 .6516 4
-6 .5708 6
-3 .1464 7
96 .55911
34 .07198
43 .32253
-3 .02258
4 .670644
2 .186405
3 .318631
2 .166362
166 .1635
105 .7603
145 .2146
165 .655
0
0
0
0
0
0
0
0
8 .739459
4 .93169
7 .472868
12 .73725
-2 .4474 9
-2 .1140 1
3 .29093 7
-3 .35791
DW
DWO
7-1-85
1
LW
LWO
DW
DWD
267 .3932
142 .0187
191 .8558
164 .7988
Appendix 3 : Nitrate and phosphate supply to Yaquina Bay vi a
riverine input and remineralization ; and removal capacit y
as calculated for macroalgal uptake .
RIVER
CONCENTRATIONS IN
SAMPLING DISCHARGE RIVER WATER (uM)
DATE
(1 E-1 )
Nitrate
Phosphate
9-9-84
425
31 .9
0 .57
9-22-84
425
29 .4
0 .51
10-6-84
935
24
0 .44
10-7-84
935
24
0 .44
12-4-84
20000
116
0 .54
1-13-85
16200
103
0 .47
3-8-85
11300
91
0 .34
4-19-85
8020
85 .26
0 .28
6-30-85
1420
71 .1
0 .54
7-1-85
1420
71 .1
0 .54
LOADING S
(mole d-1 )
Nitrate
Phosphat e
1171 .368 20 .930 4
1079 .568 18 .727 2
1938 .816 35 .5449 6
1938 .816 35 .5449 6
200448
933 .1 2
144167 .04 657 .849 6
88845 .12 331 .948 8
59079 .041 194 .019 8
8723 .1168 66 .2515 2
8723 .1168 66 .2515 2
9-9-84
9-22-84
10-6-84
10-7-84
12-4-84
1-13-85
3-8-85
4-19-85
6-30-85
7-1-85
SED REGENERATIO N
BAY-WID E
RAT E
REGENERATIO N
(umol m-2 h
)
(mole d-1 )
Nitrate
Phosphate Nitrate
Phosphate
11 .8
0
4474 .56
0
0
8 .7
0
3299 .04
34 .1
53 .6
12930 .72
20325 .12
2 .8
0
1061 .76
0 .1
0
37 .92
90 .1
34165 .92
0
5 .5
0
2085 .6
0
183
69393 .6
12 .7
0
4815 .84
9-9-84
9-22-84
10-6-84
10-7-84
12-4-84
1-13-85
3-8-85
4-19-85
6-30-85
7-1-85
REMOVAL B Y
EFFECTIV E
MACROALGAE
PHOTOPE R
(umole h-I gDW -1 )
(h)
Nitrate
Phosphate
-1 .08
-0 .28
10
-8 .8
-0 .41
9 .2
-9 .6
-0 .92
8 .7
-2 .1
-1 .8
8 .7
-3 .6
-0 .11
6 .1
-0 .23
-0 .009
6 .6
-8 .2
-0 .12
9 .2
-12 .5
-0 .55
10 .7
-35
-1 .6
12 .7
-6 .5
-0 .57
12 .3
9-9-84
9-22-84
10-6-84
10-7-84
12-4-84
1-13-85
3-8-85
4-19-85
6-30-85
7-1-85
PERCENT O F SUPPL Y
REMOVED BY MACRO
REMOVAL FACTOR
hitra*_e
Phos p hate Ni tra :e
Phosphate
1309 .9760 88 .494016
13
1
5834 .8272 15671 .347
58
15 7
1306 .9815 72 .825063
13
0 .72
37 .278352 23 .335406
0 .4
0 .23
0 .0720431 0 .2211910
0 .0007
0 .002
0
0
0
0
0
0
0
0
1 .2406260 1 .4147007
0 .01
0 .01
405 .14247 21837 .748
4
218
1003 .6005 157 .24910
10
1 .6
SUPPLY : LOADIN G
+SED REGE N
(mole d -1 )
Nitrate
Phos p hat e
1171 .368 4495 .49 0
1079 .568
18 .727 2
1938 .816 3334 .58 4
14869 .53 20360 .6 6
200448
1994 .8 8
144167 .0 695 .769 6
123011 .0 331 .948 8
59079 .04 2279 .61 9
78116 .71 66 .2515 2
8723 .116 4882 .09 1
MACRO MACR O
BIOMASS COVERAGE
(gDW m -2 )
(m 2 )
3840000
2470000
1640000
1640000
82200
0
0
274000
3560000
4380000
370
315
185
185
80
0
0
20
200
250
REMOVAL B Y
MACROALGA E
(mole
l )
Nitrate
Phosphat e
15344 .64
3978 .2 4
62990 .92 2934 .80 4
25339 .96 2428 .41 3
5543 .118 4751 .24 4
144 .4089 4 .41249 6
0
0
0
0
732 .95
32 .249 8
316484 14467 .8 4
87545 .25 7677 .04 5
e
REGENERATION 0
Nitrate
Phosphat e
+
+
+
+
+
+
+
+
+
+