JACKSON, GEORGE A. Nutrients and production of giant kelp

LIMNOLOGY
November
AND
1977
Volume 22
Number
OCEANOGRAPHY
6
Nutrients and production of giant kelp, Macrocystis
pyrifera, off southern California1
George A. Jackson
W. M. Keck Laboratories,
California
Institute
of Technology,
Pasadena
91125
Abstract
Concentrations
of nutrients in the vicinity
of the giant kelp ( Macrocystis
pyrifera ) off
San Diego, California,
varied seasonally.
Surface nitrate concentrations
were low for most
of the year (usually <l PM ), higher during winter.
Nitrate concentrations
below 4.5-m
depth usually exceeded 1 PM and were highest during spring upwelling,
lowest during
summer. Nutrients in the kelp bed were not depleted by the kelp nor enhanced by sediment regeneration,
implying relatively fast exchange between water in the bed and outside
waters. Nutrient concentrations
varied at different longshore locations.
The condition most
limiting to M. pyrifera
was probably
the low concentration
of dissolved nutrients,
especially nitrogenous
substances, near the sea surface.
Translocation
of nitrogenous
compounds by the kelp plant from depths where concentrations
are higher could compensate
for this limitation.
The summer die-off of the surface canopy may be caused by the inability of plants to translocate nutrients due to low availability
of nutrients in the deeper
water. The maximum change in dissolved oxygen measured was 0.43 mol O2 mm2between
0900 and 1130 PST; extrapolated
to 1 day this yields a production
of 1.0 mol O2 mm2 d-’
(9.5 g C rn-’ d-l).
algal protein content were found off Florida
when nutrients were highest. North (pers.
comm. ) found C : N ratios for giant kelp,
Macrocystis pyrifera, of 40 : 1 at the end of
summer and of 17: 1 in mid-December; this
change in carbon content of kelp corresponds to changes in aquatic nutrient concentration.
Nutrient supply may be important to the
large stands of M. pyrifera off California.
McFarland and Prescott (1959) estimated
the gross production of a kelp bed near Los
Angeles to be about 1 mol O2 m-2 d-l, a rate
equivalent to 12 g C m-2 d-l for an assumed
C : O2 molar ratio of 1. Towle and Pearse
(1973) calculated the production of Macrocystis off Monterey to be 7 g C m-2 d-l,
with more than 98% of it in the canopy in
the upper 3 m of the 9-m water column.
’ This work was supported in part by a training
The combination of large size and potengrant from the U.S. PHS, NIEHS (TI-ES-00004).
NOVEMBER
1977,
V. 22( 6)
LIMNOLOGY
AND
OCEANOGRAPHY
979
The availability of nutrients is one of the
primary factors regulating plant growth in
aquatic systems. Nutrient cycling has been
studied intensively in relation to planktonic
production, but although the seaweeds are
among the most productive of the marine
algae, little has been done to determine the
importance of nutrients to macroalgal production.
Topinka and Robbins (1976)
found that the growth rate and nitrogen
content of FUCW spiralis increased when
it was cultured at high nutrient concentrations. Oriental farmers increase their yields
of seaweeds by fertilizing them with ammonia or urea ( Shang 1976; Tamura 1970).
Dawes et al. (1974a,b) noted that the highest numbers of algal species and highest
980
Jackson
.
-44
\
I
\
0
I
2
3
KILOMETERS
-----I
I
117“ 18’
\
-32”s
4
DEPTH CURVE:
IN FEET
16’
30
I 7,
Fig. 1. Map _-of San
- _ Diego area. Dotted area
is Point Loma kelp bed. Naval Electronics
Laboratory (NEL)
tower is just north of entrance to
Mission Bay.
tially high productivity of kelp stands could
result in a nutrient supply inadequate to
The kelp
sustain maximum production.
bed off Point Loma (San Diego) is one of
the largest in California (about 8 x 1 km:
Fig. 1) and has been extensively studied
( North 1971b). If the production rate is
7 g C m-2 d-l, the C : N is 20 : 1 (Jackson
1975 ) , nitrogen uptake is in the top 3 m ( as
Towle and Pearse
for photosynthesis:
1973), and longshore water moves through
the bed at 10 cm s-l (Gaul and Stewart
1960) with no vertical movement, water
leaving the bed after 21 h should have lost
about 7 ,uM dissolved nitrogen. Nutrient
concentrations commonly increase with increasing depth and decreasing temperature.
Nitrate
concentration
reaches 1
PM off San Diego at depths between 10
and 50 m during spring and summer
( Strickland 1970; McCarthy and Kamykowski 1972; Kamykowski 1974). This suggests
that in the shallow waters of the Point
Loma kelp bed (mostly <15 m) nutrient
concentrations do become too low to support potential growth.
Certain processes could, however, modify
nearshore nutrient cycling.
Nutrient
regeneration in sand bottoms inshore from a
kelp bed could increase the nutrient concentrations.
Hartwig
(1974) found that
ammonia was the only important form of
nitrogen released in the sediments off La
Jolla, at an average of 870 pm01 m-2 d-l.
The compounds regenerated had a C : N
ratio of 34 : 1, high relative to phytoplankton ratios but close to that of M. pyrifera.
Nutrients may come to Point Loma from
sewage discharged by the city of San Diego. Dilution of sewage with seawater creates a water mass 3 km from shore enriched
by 7.5 PM ammonia and 0.7 PM phosphorus (SCCWRP 1975). This water mass
would be further diluted before reaching
the kelp bed. Movement caused by internal waves can affect kelp by moving nutrients vertically (Armstrong and La Fond
1966) or by changing nearshore circulation.
Semidiurnal
and diurnal internal waves
also control onshore-offshore water motion,
with water on either side of the thermocline
moving in opposite directions on and offshore (Cairns 1967, 1968; Cairns and La
Fond 1966; Winant and Olson 1976). Longshore currents are uniform through the water column, correlated with winds.
I have’ studied the relationship between
nutrients
and production in the bed of giant
kelp off Point Loma, including dctermination of nutrient distribution
in the nearshore, examination of relationships among
Nutrients
in the nearshore
981
Takahashi et al. (1970) and carbonate alkalinity calculated by the method of Strickland and Parsons ( 1968). On 8 August
1974 carbonate alkalinity
was 2.22 meq
liter-l (SD 0.03). Alkalinity
showed no
pattern in the bed.
Distributions
of nutrients were studied
with sampling stations on a transect perpcndicular to shore. It usually took 2-3 h
to complete a transect of four or five stations
through the kelp bed; during a conMethods
tinuous 24-h sampling period, transects
Bearings for sampling station positions
took 30 min when no water samples were
were obtained by sighting angles between
collected and 1 h when they were. Tranprominent onshore landmarks with a sex- sect data are displayed i.n the form of contant. Station positions were then plotted
tour plots. The contour traces were deteron a 1 : 24,000 topographical map.
mined by interpolating
between points of
Temperature,
dissolved oxygen ( DO),
known value along the sides of polygons
and pH as a function of the depth were
defined by the points.
measured in situ with a Martek Mark II
Relationships in the data were studied
water quality analyzer. The temperatureby multiple regression analysis with either
compensated oxygen electrode was stan- one or two independent variables. All varidardized in the laboratory before a sam- ables were transformed before the compupling run with air-saturated seawater at a tation of regressions to give a mean of zero
temperature of between 10” and 20°C. It and variance of 1. The assumed relationstayed within 0.1 ppm of the standard (1 ship was: x = a+ bx + cy, where x was
ppm = 6.031 mM 0,) throughout a run. the dependent variable, x and y the indeThe temperature-compensated
pH elec- penden t variables. The method estimates
trodes were calibrated in the laboratory
the regression coefficients, b and c, that
with Beckman standard pH 4 and pH 7 minimize the variance of the difference bebuffers of low ionic strength. The hydrotween the predicted and actual x.
gen ion activity measured in the field was
Point Loma is the peninsula forming the
used to calculate the total inorganic carbon
western boundary of the entrance to San
(CT) in solution for a constant alkalinity
Diego Harbor ( Fig. 1). The bottom on the
of 2.22 mcq liter-l by using the appropriate
offshore side is a rocky shelf extending out
equations and stability constants given by 2 km to a depth of 20 m before dropping
Stumm and Morgan (1970) [pKI = 6.11off rather sharply. Interspersed on the
O.O06(T-5),
pKa = 9:34-O.Oll(T-5)].
shelf are rocks rising up to 10 m off the
Water samples for nutrient analysis were
collected by a diver within 1 m of the bottom and patches of sand. There are
probe, stored in polyethylene bottles and more sand and rock outcrops inshore.
The kelp bed extends from 1.5 km south
frozen with Dry Ice for storage. Nitrate
plus nitrite, phosphate, and silicate were to 7 km north of the tip of Point Loma.
measured according to Strickland and Par- North of Point Loma is Mission Bay, the
sons (1968). A mmonia was measured by NEL ,tower, and La Jolla. The density of
the method of Solorzano ( 1969). EN was plants is about 0.3 plants per square meter
calculated by summing the concentrations
(P. Dayton pers. comm. ) . There was a
of ammonia, nitrate, and nitrite,
heavy surface canopy throughout my study.
Samples collected for alkalinity measureMacrocystis is one of the largest of the
ments were kept cool, not frozen, Total al- seaweeds. A mature plant will have 40 or
kalinity was measured by the method of more fronds in various states of growth
dissolved nutrients, oxygen and inorganic
carbon, and estimation of production on 1
day.
I thank W. J. North, J. J. M,organ, I-1.
Lowenstam, D. Checkley, T. Sibley, L.
Quetin, and R. R. Quetin for their help during this work. I also thank J. Teal and B.
Nicotri for critically
reading the manuscript.
982
Jackson
DISTANCE TO SHORE(km)
0
I.8
1.6
1.4
1.2
DISTANCE TO SHORE (km)
1.0
2
4
36
’
F
48
a
0.24,
0.21 +
IO
12
14
0
2
g4
F6
El
cl 8
IO
12
14
I
//
0.8’
-1
Fig. 2. Water properties through kelp bed 1.8 km north of Point Loma tip at 1400 PST, 27 May
1975. Kelp bed extended from 1.1 km to 1.8 km offshore.
Locations
sampled shown by +.
A12.9”-17.1”C;
B-dissolved
oxygen distribution,
0.16-0.40
mM; C-phosTemperature
distribution,
phate distribution,
0.21-0.88 ,uM; D-nitrate
distribution,
0.3-4.8 PM.
attached to the rootlike holdfast. A frond
is similar to a vine, can be as long as 25 m
and have as many as 300 blades attached
along the stipe. Bundles of stipes rise from
their holdfasts to the surface, spreading
out to form a canopy. Beds often reach
wet weight densities of 6 kg m-2; as much
as half of this can be in the canopy (Towle
and Pearse 1973; McFarland and Prescott
1959).
Results
TypicaZ patterns-1 sampled the kelp bed
from 1972 to 1975 on 13 occasions at different times of the year.
Figure 2 shows isopleths of various properties for a slice through the kelp bed on
27 May 1975. The transect ran perpendicular to shore 2 km north of the tip of
Point Loma. The outermost station was at
Nutrients
in the nearshore
983
the outer edge of the kelp bed, the inner
DISTANCETO SHORE(km)
station inside the bed near the inner edge.
‘7
I;’
1; : Ii5 : yI
I.3
1.2
This was a typical sample taken near local
*
+
-c=noon when photosynthetic
rates should
+
+
+Ihave been maximal.
The temperature map (Fig. 2A) shows
stratification
without
the typical pattern:
a sharp thermocline. The depth of an isotherm varied by as much as 5 m at the different stations as a result of short-period internal waves moving through the kelp bed
(Lee 1961; Quast 1968).
The dissolved oxygen contours ( Fig. 2B)
are similar to the temperature contours:
oxygen concentrations decreased with in-I+
+
creasing depth. In addition, the highest
1.
14’
L
oxygen concentrations were near the surdistribution,
0.14Fig. 3. Dissolved
oxygen
face in the midst of the kelp bed.
Phosphate contours (Fig. 2C) for the 0.25 mM, at 0500 PST, 28 May 1975. Stations
same as in Fig. 2.
diurnal sampling show significant gradients
in concentration even in the relatively shallow bottom depths of the kelp bed, <15 m twecn changes of nutrient patterns caused
deep. The phosphate concentration at the by open ocean phytoplankton
and nearsurface was <0.3 PM, but 0.8 PM at the shore benthic plants.
bottom. Despite the strong gradient, the
Nutrients showed the same vertical disamounts of phosphate at the surface were tribution several kilometers to sea that they
still significant. Phosphate was also always
did in the outer edge of the kelp bed. This
present at about these concentrations in my is the common pattern for the local waters
other samplings.
( e.g. Strickland 1970).
The dominant form of inorganic nitrogen
There did not seem to be marked effects
in the bed was nitrate. Nitrate concentraby the kelp bed on the measured parametions for the diurnal sampling also showed ters except for dissolved oxygen concentraa strong vertical gradient ( Fig. ZD), <0.5 tions. It was therefore of interest to see
PM at the surface and >4.5 PM at the bot- whether the large kelp biomass would cause
tom. Nitrate concentrations were very low the oxygen content of the water to fall sigat the surface, relatively lower than phos- nificantly during the night. Comparison of
phate. Surface nitrate concentrations be- oxygen concentrations
in the bed with
low 0.1 ,L~M were common during the 4 those outside to determine the extent of
years of this study.
oxygen depletion by kelp respiration for
Ammonia also displayed vertical concen- 28 May 1975 shows no appreciable deprestration
gradients;
concentrations
were sion of oxygen levels ( Fig. 3).
never as high as those of nitrate, rarely surSeasonal
nutrient
patterns-Nutrient
passing 1 PM. Ammonia was sometimes a stratification in the kelp bed varied seasonsignificant fraction of the nitrogen in the ally. The annual cycle is shown by comparing the median- value of the nutrient
upper meters of the kelp bed when nitrate
concentrations went to zero.
samples taken bctwecn 0- and 4.5-m depth
Silicate showed concentration gradients
to the median value of the samples taken
similar to those of phosphate, nitrate, and between 4.5 and 9 m for all of the days
ammonia. Since silicate should not be taken sampled (Fig. 4).
The temperature at the surface and beup
to any significant degree by M. pyrifera,
it is a convenient tracer to distinguish be- low shows the same pattern that Cairns and
984
Jackson
DISTANCE NORTH OF PT. LOMA (km)
0’
2 0.6r
’
’
’
e:\ m ’
’
n ’
’
n ’
I ’
I \
$;kLM,
JFMAMJJASONDJ
MONTH
Fig. 4. Annual
cycle of nutrient
conccntrations. Solid IincsL-median
concentrations
of samples gathered between surface and 4.5-m depth;
dashed lines-median
concentrations
of samples
gathered between 4.5 and 9-m depth.
Fig. 5. Water properties
along 20-m bottom
contour between Point Loma and Point La Jolla
durjng an upwelling
event, 6 May 1975. A-Temperature
distribution,
10.4”-15.8”C;
B-nitrate
and nitrite distribution,
0.4-16.5 ,uM.
Nelson ( 1970) found at the NEL tower:
there is stratification between March and
November.
The amount of stratification
varied with the season but this is not clear
from Fig. 4.
Surface concentrations of nitrate were
low for most of .the year. Median conccntrations in the upper 4.5 m of the water column were <1 PM from April to November,
except for an upwelling event on 6 May
1975. In winter, the surface nitrate concentrations did rise. Below 4.5 m they were
higher, although for much of the year the
concentrations in the deeper water were
<2 PM. The major exceptions were that in
March, April, and May-the
upwelling
months (Jones 1971; Bakun 1973)-nitrate
concentrations were low at the surface and
high below. That is, during the time of
maximum kelp growth, nitrate concentrations were low at the surface where most of
presumably
occurs.
the photosynthesis
The high concentrations ‘of this important
nutrient lay below 4.5 m.
The other nutrients also showed higher
concentrations in the lower parts of the kelp
bed. Ammonia, however, never achieved
the high concentrations displayed by nitrate. The highest median concentration of
ammonia measured was 0.8 PM on a day
when the median nitrate concentration was
10 PM. The lack of anomalously high ammonia concentrations suggests that the San
Diego sewer outfall was not an important
source of nutrients. The median concentration of phosphate never dropped below
0.2 PM. During the upwelling
months
phosphate concentration
did rise in the
deeper parts of the bed.
Thus there was a seasonal distributional
pattern common to all the nutrients. Concentrations were always higher in nonwinter months at depths >4.5 m, although the
difference between surface and deeper wa-
Nutrients
in the nearshore
DISTANCE
TO SHORE (km)
I
I
I
I
I
I
I
I
AT OCEAN BEACH PIER ,039
4km TO SEA: 0 13
,
I
\
I
b
OCEAN EEACk PIER:0.09,0.07
I 46
:+
I
I
I
t
I
I
I ‘$0
--I-----
--
-I-I
l
1,I
I
Ihrn--’
I
‘1,
\
7
\
06l+
-
‘1
\
o,36 0.25 “‘“2
+
+
\
\
\
\
Fig. 6. Nitrate concentrations
of surface _- sam-plcs. A-Collected
20 April 1972; B-collected
23 May 1972. Dashed line perpendicular
to coast
-sewer
outfall;
dashed lines parallel to shoreedges of kelp bed.
ters was not always great. The sharpest
vertical changes occurred during the period
which has historically
been the time of
greatest kelp growth and of strongest upwelling.
During much of the rest of the
differences
between
year, concentration
the surface and the deeper waters were
small. The nutrient that seemed to be in
shortest supply was nitrogen. During winter the vertical gradients were small and
the surface concentrations of nitrogen and
phosphorus higher than in summer.
Longshore patterns--I
ran a transect
parallel to shore, along the 20-m bottom
contour, on 6 May 1975 to determine
whether differences in nutrient distribution
occurred along the coast.
, The temperature
contours (Fig. 5A)
showed no stratification of the water at the
tip of Point Loma, where the water was
cold from the surface to the bottom. Stratification appeared between 3.5 and 4.5 km
north of the tip. The water was markedly
stratified, with a vertical temperature gradi-
Fig. 7. Water properties through kelp bed on
transect 0.6 km north of Point Loma tip, 9 July
1972. Kelp bed extended 1.1-1.9 km from shore.
A-Nitrate,
PM; B-ammonia,
PM; C-tcmperatrue, “C.
ent as large as 1 “C m-l, 12 km north of
the tip. Nutrient distribution was affected
by this upwelling.
Surface nitrate concentrations were high at the tip of Point Loma
( Fig. 5B ) while at the same time there
were low surface and high bottom concentrations of nitrate around La Jolla.
On 23 May 1972 surface nutrient concentrations were also higher to the south
then to the north of Point Loma. Surface
nitrate concentrations within 3 km of the
tip were almost all between 0.6 and 0.2 PM
(Fig. 61))) while at all northern stations (5
km from shore, in the kelp bed 5 km north
of the tip of Point Loma, and at the Ocean
Beach Pier) they were <O.l ,uM. Although
these were not great differences on an absolute scale, the nitrate concentrations to
the south were frequently more than five
times as great as those farther up the coast.
Data from 20 April 1972 indicated that nutrients near the tip of Point Loma are not
always higher (Fig. 6A). On that date
986
Jackson
Table 1. Oxygen-ammonia
and oxygen-nitrate
relationships,
both uncorrected
and corrected
for
phytoplankton-induced
relationships
( Eq. 1) . The regression coefficient,
p, is presented with standard
error of estimate.
Regression coefficients
are in units of micromole
per millimole.
AO, : ANIL and
AO, : ANOB ratios arc in units of mole per mole.
9 JuL
Sample number
16 Apr
21 May
8 Aug
20 Sep
14 Nov
37 May
1972
1972
1974
1974
1974
1974
1974
1974
1975
31
29
15
16
31
28
32
22
112
-0.10
-0.7
1.4
1492
-0.63
-4.1
1.4
244
-0.72
-4.8
1.2
208
0.84
3.6
0.4
-278
-0.80
-3.4
0.5
299
-0.66
-2.2
0.5
459
-0.38
-1.3
0.7
781
-0.73
-3.4
0.3
294
0.89
-2.0
0.6
508
0.80
-3.4
0.5
295
0.66
-2.1
0.5
488
0.38
-1.3
0.8
752
0.75
-3.2
0.3
316
-0.87
-60
-0.49
-11
-0.01
-0.1
-0.47
-22
17
89
-9.65
-13
3
78
0.91
-37
0.98
-4
1
256
0.92
-7
2
151
NH4(pM) fn 02(mM)
r
-0.41
-1.5
T
SE
0.6
-A02:ANH
685
4
NH4(pM) --fn O,(mM), Si(vM)
21
Nov
24
Feb
;
SE
-A02:ANH4
N03(uM) fn_ 02(mM)
r
-ii
SE
-A02:AN03
N03()1M)
fn
02(mM),
-0.65
-3
6
36
0.07
9
26
-0.72
-78
20
13
-0.93
-58
6
17
6
45
Si(uPf>
$
SE
27
-A02:AN03
there were no significant longshore differences between the kelp bed areas sampled
along the Point Loma peninsula.
Onshore variations--rThe highest surface
nitrate concentrations on 20 April 1972, 1.46
and 1.0 PM, were from samples taken near
to shore ( Fig. 6A). The ammonia concentrations at those two high-nitrate
stations
were <O.l PM. Thus the high values were
not caused by regeneration from the sediments but were possibly the result of wave
induced mixing or shallow water transport.
Further relevant data (some shown in
Fig. 7) come from samples taken on 9 July
1972, when the transect extended from 0.2
to 2.8 km offshore. The shallowest station
was in water about 6 m deep, in an area of
intense wave surge. The nutrient concentrations at this station, at the surface and
at the bottom, were: nitrate, 4.2 and 4.3
PM; ammonia, 0.4 and 0.4 PM; and phosphate, 0.48 and 0.42 PM. This contrasted
sharulv with the other stations, which had
0.94
-9
1.6
112
20
40
~~py$g
J
FMAM
J
J
ASONDJ
MONTH
Fig. 8. Annual cycle of nutrient uptake ratios.
Ratios are regression coefficients
for dissolved species; error bars are standard error of estimates.
Nutrients
40’
I
0123456
I
I
I
I
I
0123456
MEDIAN N CPM)
MEDIAN N tpM)
Fig. 9. Nitrogen
uptake
12 m; B-O-4.5
m.
ratios
as a function
of median
a maximum concentration of nitrate at the
surface of 0.13 PM. There were, however,
high nitrate concentrations away from shore
below 10 m, with the maximum measured
being 9.5 ,u~cM.
Chnnges in nutrient and oxygen concentrutions-The
extent of nutrient
uptake
during kelp photosynthesis
and growth
should be mirrored in the ratios between
the oxygen and nutrient concentrations of
the nurturing
seawater. Ratios between
dissolved nutrients and oxygen in kelp bed
waters are determined not only by kelp
growth but also by previous phytoplankton
growth. The extent to which phytoplankton influence the oxygen-nutrient
relationship can be determined by using silicate as
a tracer of phytoplankton
nutrient uptake,
The relationship assumed was
[nutrient]
987
in the nearshore
= a + p[O,]
(+y[Si]).
(1)
Coefficients (a, & r), their standard errors, and correlations were determined by a
multiple linear regression program. Regressions that included silicate as a variable
were considered to be corrected for phyto-
inorganic
nitrogen
concentration.
A-4.5-
plankton effects. The A(nutrient)
: AO2 ratio is p, and AO2 : A( nutrient) is its inverse.
The importance of different inorganic
forms of nitrogen in supplying
growth
240
220
200
zs
s
0”
180
160
140
-6
- +A
/”
I vfOA’
‘2010
II
12
I
I
I
I
13
14
15
16
17
T (“Cl
Fig. 10. Relationship
between
dissolved
oxygen and temperature,
transect 1, 21 May 1974.
Line fit by least-squares
is [O,( mM)] = -0.085
+ O.O194T( “C),
T = 0.95. Sampling
times and
station distances for transect 1: station 1 (+ )0730 PST, 1.7 km; station 2 (C))--U830
PST, 1.5
km; station 3 (A )-0900
PST, 1.2 km.
988
Jachon
AO,(tLM)
-100
-60
- 20 n
/’
20
60
o
MEDIAN ZN&M)
2 4 6 8 IO I2
/
8
-ST5
IO
ST 7
12
Fig. 11. Depth dependence on 21 May 1974. A. Oxygen changes on transect 2, calculated
as
difference between mcasurcd oxygen concentration
and concentration
predicted
for that temperature.
Sampling times and station distances for transect 2: station 4 (+ )-lo55
PST, 1.92 km; station 5
( x )-1110
PST, 1.56 k m; station 6 (O)-1125
PST, 1.32 km; station 7 (El)-1210
PST, 0.72 km;
station 8 ( n )-12X
PST, 0.5 km. B. Median ZN concentration
as a function of depth.
needs of the kelp bed can be determined
by comparing changes in the nitrogenous
constituents as a function of the changes
in oxygen concentration. The -AO2 : ANI14
ratios, corrected for phytoplankton
effects,
had a median of 488 (n = 5; range, 295752) ( Table 1). Uncorrected, the median
ratio was 299 (n = 9; range -278-1,492).
The changes in nitrate concentration were
much greater, with the corrected -AO2 :
ANOa ratio having a median of 132 (n = 4;
range, 27-256), and the uncorrected ratio
having a median of 36 (n = 7; range 1389). I conclude that more nitrate was
taken up than ammonia and therefore that
nitrate was more important than ammonia
as a nitrogen source to the kelp.
The corrected ratios, having had the
lower 8 : 1 C : N phytoplankton
ratios factored out, are higher than the uncorrected
ratios, but the patterns are similar.
The seasonal variation of AZN: AO2 resembles that of the previously discussed
median nitrogen concentration
( Fig. 8).
AEN: AO2 values are most negative during
early spring. The correlation of AXN : AO2
is highest for the median concentration of
total inorganic nitrogen between 4.5 and
Nutrients
989
in the nearshore
10.5 m below the surface (n = 9, r = -0.83).
The correlation is lowest for the median
nitrogen concentration at depths between
the surface and 4.5 m (Fig. 9: n. = 9, r =
-0.51) , Correlation was intermediate
for
the median nitrogen concentration in the
water from the surface to 10.5-m depth (n
=9, r=-0.65).
ProcZuc-tion-I measured oxygen concentrations in the kelp bed at two different
times on 21 May 1974. I could not calculate kelp production by subtracting midday
oxygen concentrations from those of the
early morning because the vertical temperature distribution changed in the 2-3 h
between sampling runs. It was thus not
reasonable to assume that all water motion
was simple and horizontal. Dissolved oxygen concentration
and temperature were
highly correlated for the early morning
samples (Fig. 10).
I assumed that deviations from this
linear relationship
for water sampled at
midday (Fig. 11) were caused by kelp
production.
The greatest oxygen change
was 0.43 mol O2 m-2 in the middle
of the kelp bed (sta. 6) at 1125 PST.
This station, 0.6 km from the offshore
and onshore kelp bed edges, would
have been least affected by water movement. Measurements taken between 0730
and 0930 PST showed little evidence of
photosynthesis.
The oxygen change was
the result of an average production rate of
at least 0.17 mol 02 m-2 h-l. If this rate
were maintained, and if all production were
between 0900 and the time when the sun
dropped to the same sky angle ( 1500),
then production would have been 1.02 mol
02 m-2 d-l. This is equivalent to 9.5 g C
m-2 d-l for a -AO2 : AC ratio of 1.30 (Fig.
12). Kelp respiration
can be estimated
from Sargent and Lantrip’s ( 1952) rate of
1 ml 02 g-l wet wt d-l. If the Point Loma
kelp density (wet wt) was 6 kg m-2, the
respiration was 0.27 mol O2 m-2 d-l.
Discussion
Production measurements are never easy.
Oceanic measurements have been made
mainly by measuring carbon fixation in wa-
0.3
0.2
0. I
2.1
2.2
2.3
C,(mM)
Fig. 12. Dissolved
function
of inorganic
mation in Table 2. )
oxygen
carbon.
concentrations
(Regression
as a
infor-
ter samples containing phytoplankton.
The
range of light, nutrient, temperature, and
water motion conditions that different parts
of a single kelp plant respond to makes
simulation of natural conditions almost impossible. Towle and Pearse (1973) calculated gross kelp photosynthesis by measuring carbon fixation of blades isolated in
bags. However, bags stop the flow of water
over blade surfaces and should cause a decrease in photosynthesis.
McFarland and
Prescott (1959) calculated gross and net
production after measuring diurnal oxygen
concentrations and surface currents in a
kelp bed. They measured currents at the
surface and at i-m depth every 3 h but assumed that water flowed parallel to shore.
They found oxygen changes that did not
fit their model and had to ascribe them to
water intruding into the kelp bed. In the
absence of accurate measurements of current throughout
the water column, their
production-values
must remain suspect.
990
Jackson
I found the greatest oxygen changes not at
the surface but between 3- and 6-m depth.
One would expect to find the maximum
photosynthesis at the surface: McFarland
and Prescott found 35-50% of the blade
arca at the surface; To&
and Pearse
found 71% of the blade mass and 99% of
the photosynthesis there. In addition, light
intensities are highest at the surface. However, McFarland
and Prescott also observed that the highest oxygen changes
were 3 m below the surface.
Loss of oxygen to the atmosphere from
supersaturated
waters near the surface
could account for the relatively low dissolved oxygen concentrations there. If the
atmosphere were an important sink of oxygen, surface waters would be deficient in
oxygen for a given concentration of inorganic carbon ( C, ) . A plot of dissolved
oxygen versus dissolved inorganic carbon
would show a region of constant oxygen
concentration at low CT, caused by escape
of oxygen without
an input of carbon.
There was no such relationship on 21 May
1974 (Fig. 12) nor on any other day that
I examined (Jackson 1975). Thus, a significant amount of oxygen was not going to
the atmosphere from the kelp bed.
Oxygen changes could be greater at 3
m if photosynthesis predominated
at the
surface and if the water at 3 m had been
at the surface longer than the warm water
layer that forced it down. This explanation
would not account for the high oxygen increases also present at 61m at both stations
6 and 7 (Fig. 11). Most photosynthesis
would occur below the surface, despite
low light levels and photosynthetic area, if
low nutrient supply inhibits photosynthesis.
On 21 May 1974, nitrate concentrations
were again low at the surface and higher at
3- and 6-m depth. This suggests that photosynthetic rates are indeed related to nutrient concentrations.
Oxygen : nutrient ratios provide further
information
about nutrient
effects on
growth, Redfield et al. ( 1963) related the
amount of oxygen produced by marine algae to the amount of inorganic carbon and
nitrogen that they take out of solution and
incorporate in tissue:
AO2 = -AC, - 2AN03.
(2)
This implies that
(AC, : ANO,)
= -(AO,
: AN03) - 2. (3)
Because the oxygen and carbon ratios can
bc related, changes in dissolved oxygen and
nutrient concentrations can be compared
with the known carbon : nitrogen values of
M. p yriferu.
Nutrient : ‘oxygen ratios show that kelp
plants take up relatively more nitrogen at
times of higher nitrate concentration (Figs.
8, 9). AO2 : ACT ratios of about -1 should
be another indicator of low nitrate uptake.
This relationship holds moderately well for
the available data (Table 2). We infer that
plants have their highest internal nitrogen
concentrations
during those times when
ambient nutrient concentrations are highest. During times of low ambient nutrient
content
plant
nitrogen
concentrations,
drops, possibly slowing the growth rate.
Thus far I have assumed that the primary
source of nitrogen for kelp is nitrate. Are
the organic forms, the most important of
Table 2. Comparison
of oxygen and inorganic
Regression
coefficients
carbon regression ratios.
are in units of millimole
per millimole.
AO1 : AN
and AC : AZN are in units of mole per mole. For
[nutrient]
= p + XCh.
carbon, equation
fit was:
3
Jul
'72
o,(M
fn cpm
r
_x
SE
24Feb 16Apr 21?Iay 8 Aug
'74
'74
' 74
'74
-0.94 -0.93 -0.95 -0.90 -0.90
-0.98 -1.36 -1.02 -1.30 -1.64
0.07 9.14 0.08 0.11 0.15
CN(pM) -fn 02(mM)
:
-0.67
-29 -0.74
-82 -0.93
-63 -0.87
-64 -0.58
-15
SE
6
21
7
7
4
-35
-12
-16
-16
-69
33
10
14
14
67
-A02:ACN-2
A02:ACN
CN(pM) fn C,(mFl>
r
0.63 0.74 0.91 0.93 0.62
30 126
68 104
25
T
SE
7
30
8
7
7
34
8
14
10
36
AC:ACN
Nutrients
in the nearshore
which seems to be urea, important to the
growth of kelp? The evidence suggests
that urea, at least, is not. McCarthy ( 197.1)
found that the concentration of urea in seawater was usually <1 PM. This is the magnitude of the concentration of ammonia in
the kelp at Point Loma. It is doubtful that
urea
serves as an unknown, highly significant source of nitrogen for Macrocystis at
Point Lomn because ammonia, which is
taken up prcfcrentially
to urea by algae,
was not an appreciable nitrogen source for
the kelp and was not totally depleted in
the surface.
It should not be surprising that the photosynthetic production by M. pyrifera is
strongly influenced by the nutrient conccntration of the surrounding water. Fluctuations in growth patterns of the alga could
be explained by spatial and temporal variation in distribution of nutrients.
North (1971a) has often observed that
surface parts of kelp fronds deteriorate during summer months, The parts of the kelp
bed below the thermocline usually remain
healthy. Since many of the very productive brown algae are found in areas of cold
water, the conclusion has often been made
that temperature determined the growth of
these seaweeds (e.g. North 1971a). However, when Clendenning ( 1971) examined
the effect of temperature on rates of photosynthesis and respiration of M. pyrifera, he
found that the plants had a favorable photosynthesis to respiration ratio for temperatures at which tissue damage was observed
in the field. He concluded that the temperature-linked
die-off of the surface canopy was not due to an adverse change in
the photosynthesis : respiration ratio among
surface blades. Die-off association with
high temperatures suggests a cause-andeffect relation. The die-off could also result, in part at least, from low nitrogen
concentrations in the water above the thermocline and possible temperature-nutrient
interactions.
A compilation
of my data
shows that high temperature and low nutrient concentrations are indeed related (Fig.
13). Evidence that the die-off is caused by
high temperatures is at present insufficient,
Fig. 13. Relationship
bctwecn temperatme
total inorganic
nitrogen,
Point Loma kelp
1972-1975.
991
and
bed,
If canopy die-off is caused by low concentrations of nitrogen in the surface water
during summer, the question remains of
what allows the canopy to grow during the
other months. It is only during summer
that the concentrations in the deeper parts
of the kelp bed decrease. The probable
explanation involves translocation of nitrogen from deeper parts of the plant bathed
in higher nitrate water. Parker ( 1963, 1965,
1966, 1971; Parker and Huber 1965) has
examined the physiological basis for transport in M. pyrifera. Translocation occurs
in a tissue very similar to the phloem of
land plants. Organic matter is translocated
along the stipe toward the growing tip and
toward the base from photosynthetic tissues
in the middle of a frond. The predominant
transport is toward the growing tip at the
apex at rates as great as 80 cm h-l. This is
equivalent to a volume flow rate of 1 ml
h-l (Jackson 1975).
Parker ( 1966) analyzed the translocated
fluid and found that the dominant carbon
compounds were mannitol and free amino
acids (Table 3). The total concentration of
carbon in the fluid was 2.07 molar, of nitrogen 0.23. Ammonia forms a negligible frac-
992
Jackson
Table 3. Content of translocated
kelp fluid.
For protein and undetermined
amino acid fractions,
molecular weight assumed to be 125/( amino acid residue),
nitrogen content assumed l/residue,
and
carbon content assumed 4/residue.
Concn.
Molecular
(s/d
Total solids
D-mannitol
protein
lipid
total
aminc acids
L-alanine
asPartic
acid
glutamic
acid
citrolline
other
148.9
36.0
19:1
?:6
No. N/
No. C/
wt.
molecule
molecule
(mM)
(mM)
1%
$125
0
SL1
6
Q4
4:
1254
184
1
1
3
4
a9
9.83
2.63
1.45
0.43
4.7
131
147
175
%125
:
Ql
z
SL4
Total
110
20
10
383
227
C:N (molar)
C:N (weight)
tion of the nitrogen (Jackson 1975). The
flux of nutrients in the phloem could be 2
mmol C 11-l and 0.2 mmol N h-l, equivalent
to 24 mg C h-l and 2.8 mg N h-l. The
C : N ratio of this fluid is 9 : 1 on a molar
basis. Analyses of kelp show that the tissue
has a C : N ratio varying between 12 : 1
and 50 : 1 ( North pers. comm. ) . Thus, the
translocated fluid has a greater relative
concentration of nitrogen than the whole
plant.
When surface blades cannot take suffi-
IO
Concn.
+
1
I
I
1
O,(mM)
Fig. 14. Total N vs. dissolved oxygen, 9 July
1972. At low inorganic
nitrogen
concentrations,
there was oxygen evolution without corresponding
O-surface
samples.
nitrogen uptake.
= 2068/227
= 7.81
N
Concn.
C
330
80
1”:
152
2068
= 9.11
cient nitrogen from solution, they could be
using nitrogen translocated from below.
The relationship between oxygen and total
nitrogenous substances shows that tissues
in the low nutrient surface waters do not
always absorb nitrogen in amounts corresponding to their oxygen production (Fig.
14). On 9 July 1972, the decrease in total
inorganic nitrogen corresponding
to the
0.15 mM increase in dissolved oxygen
would have been 3 PM for a plant producing tissue with a C : N ratio of 50 : 1. The
highest surface concentration around the
bed that could have been drawn on was
0.5 PM. The implication is that the surface
tissues depend on translocated nitrogen for
their growth.
Because the C : N ratio of the translocated fluid is 9 : 1 and the C : N ratio of
summer surface blades is about 45 : 1, at
least a fifth of the carbon for growth at
the surface would have to come from tissue
in deeper water. If fluid is translocated to
the surface, where tissue is being produced
at a rate of 24 mg C h-l, then one frond
could be photosynthesizing
at a rate of 120
mg C h-l. At a stipe density of 4 m-2 and
for an 8-h day, the production associated
with translocated nitrogen would be 4 g C
m-2, This is quite close to the 2.5 g C m-2
Nutrients
in the nearshore
d-l measured in the surface 3 m at a ime
when the canopy seemed nutrient limited.
Presumably the lower parts of the plant
cannot translocate enough nitrogen to the
surface and the canopy dies back when
either the nitrogen concentration
or the
light intensity becomes too low. This dieback would then permit more light to penetrate and thus increase the photosynthetic
rate of the lower parts of the kelp. Perhaps
there are also other algae that are adapted
to grow at times when the canopy dieback
allows more light to reach the bottom,
where they reside in seawater with higher
nutrient concentration
than the surface.
When canopies inhibit photosynthesis in
deeper tissues, harvesting
the canopy
might increase kelp growth in the understory.
A plant with stored nitrogen should have
tissue with a relatively low C : N ratio.
Such a plant would be able to fix carbon
without an outside nitrogen supply. When
the internal nitrogen supply becomes deplcted, the plant can no longer grow. The
seasonality of C : N values in Macrocystis,
varying from 17 : 1 in winter to 40 : 1 at the
end of summer, suggests some storage of
nitrogen. Whenever the plant acquires carbon and nitrogen from solution in a ratio
greater than 40 : 1, it depletes its internal
nitrogen reservoir. When the C : N value
of the plant reaches 40 : 1, presumably
there is no reservoir left and tissue carbohydrate
capacity
is saturated;
further
growth by surface tissue must be supplied
by nitrogen from translocation. Under even
lower nutrient
conditions, carbon might
also be fixed and released back into seawater as organic compounds; this possibility should be investigated.
Conclusions
The distribution of nutrients in the nearshore is similar to that in deeper oceanic
areas. The thermocline may be shallower
in the nearshore but there are still large
vertical gradients in nutrient concentrations. The nearshore exchanges water with
the oceanic zone faster than the kelp can
993
significantly
decrease, or sediments increase, nutrient concentrations.
Thus the
nearshore nutrient regime is closely linked
with the oceanic. Along the coast there are
differences in nutrient regimes involving
localized upwelling
effects, greatest near
projecting points of land (e.g. Armstrong
et al. 1967). The importance of effects related to upwelling in the nearshore implies
that large-scale wind patterns are influential here.
The close nearshore (depth <5 m) also
seems to be different from the general nearshore. My data are not extensive enough
to define the extent of such mechanisms
as wave mixing or longshore transport in
determining the higher nutrient concentrations in shallow water.
There are remarkably few changes in the
various water propertics measured in the
kelp bed, The strong exception is the daytime oxygen concentration
in the upper
waters. The surface nitrogen concentrations
are not reduced by amounts that a simple
analysis predicts. However if nitrogen uptake is spread throughout the water column
and is not directly related to photosynthesis, then changes in nutrient concentration
can bc expected to be smaller at the surf ace. This would be necessary if the plants
at the Point Loma kelp bed, with low concentration of nitrate, and ammonia at the
surface, are producing at the rates reported
for the Monterey Bay stand.
Nutrient patterns do indicate that the
nearshore is divided into areas with diffcrent nutrient regimes. Phytoplankton growth
studies have shown great differences in the
ability of different species to utilize nutrients at low and high concentrations, and
these different
nutrient
responses have
been used to explain algal assemblages in
nut.ricnt-rich upwelling areas and in &gotrophic central oceanic gyres (Eppley et
al. 1969). Similar differences among seaweeds could influence their ability to compete and hence their distribution,
For seaweeds, however, the rate of nutrient supply is determined not only by nutrient concentration, as it is for phytoplank-
994
Jackson
but also by water motion
(Mu&
and
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