CARBON DIOXIDE
DYNAMICS:
A RECORD OF ORGANIC
CARBON PRODUCTION,
RESPIRATION,
AND
CALCIFICATION
IN THE ENIWETOK
REEF
FLAT COMMUNITY’
S. V. Smith2
Dcpartmcnt
of Oceanography
and Hawaii Institute
of Geophysics,
University
of IIawnii,
IIonolulu
96822
AIXTRACT
Organic carbon production,
respiration,
and calcification
alter the CO:! content of water
crossing the Eniwctok windward
reef flat. Changes in pII and total alkalinity
can be used
to partition
the CO, chnngcs into those due to production-respiration
and those due to
calcification.
Gas transfer across the air-sea intcrfnce is minor.
Both a transect visually
dominated
by a mixture of corals and algae and a transect
dominated by an algal turf calcified at an avcragc rate of 4,000 g CnCO,, n-” yr-‘, with no
apparent day-to-night
difference.
Although
nighttime
rcspirntion
on both transects was
0.12 g C m-” hr-‘, the algal transect exhibited a much higher daytime net production
rate
than did the coral-algal transect ( 0.72 vs. 0.25 g C m-’ hr-’ ) .
Although little particulate
&CO.: was removed From the reef flat during these stuclics,
thcrc has been virtually
no net C&O:, accumulation
there over the last several thousand
years.
An organic reef builds a calcarcous structure as its most conspicuous product. Not
only dots this structure greatly modify the
surrounding environment, but it also provides a prominent gcologicnl record of the
reef history. The structure is ample proof
that calcification is an important metabolic
process of the reef community, yet information on reef calcification rates is sparse and
conflicting.
In an effort to sort out the available information on ClaCQ3 production in coral
reefs, Chave ct al. ( 1972) applied the terms
potential production
to the calcification
rate of an organism, gross production to the
production rate of the community, and net
production to the CaC03 retention rate of
the reef. C80mmunity ( or gross ) production
’ IIawaii
Institute
of Geophysics
Contribution
No. 434. Contribution
of the Eniwctok
Marine
Biological
Laboratory.
This rcscnrch
was pcrformed using the facilities of HV Alp& Helix and
of the Eniwetok Marinc Biological Laboratory.
The
rcscarch was supported by Atomic Energy Con)mission Contract No, AT-( 29-2”)-226 and by funds
from the National
Scicncc Foundation
and from
the Janss l?ounda tion.
IIawaii
Institute
of Marine
’ Prcscnt address:
Biology, P-0. Box 1340, Knneohc
96744.
LIMNOLOGY
AND
OCEANOGRAPIIY
has been evaluated previously by summing
the product of potential production times
reef proportion covered for each of the reef
components. My study addrcsscs the problem of estimating gross production more
directly by monitoring the chemical effects
of reef calcification on the CO2 system of
adjacent waters.
I th.ank my colleagues both on the Symbios Expedition and at the University of
Hawaii for their considerable assistance. I
particularly
thank R. E. Johannes, W. J.
Wiebe, M. E. (2, I’ilson, D. W. Kinsey, G.
S. Key, and K. E. Chavc for their comments
S. D. Hicks supplied
on this manuscript.
data on sea level at Eniwetok.
HISTORIC
AND
GEOGRAPHIC
SETTING
Sargent and Austin (1949, 1954) were
the first to assess reef metabolism from
changes in the composition of water flowing
across a reef flat. Their study was conducted on a windward reef flat at Rongclap
Atoll, Marshall Islands. Incidental to their
study of organic metabolism was an cstimatc
of the coral calcimass on the reef (44,000
g CaC’& n-2) and estimates of coral
growth in Samoa dcrivcd from Mayor
106
JANUARY
1973, V. 18(l)
ENIWETOK
IIEEF
FLAT
CO2
107
METRl3OLISM
1
_ II 030’
N
TRANSECT LOCATIONS
WINDWARD SIDE ENIWETOK
ATOLL
MARSHALL
ISLANDS
METERS ON TRANSECTS
SHOWN BY SQUARE
DUM 8 ODUM (1955) TRANSECT
ALSO SHOW1
MAY-JUNE
1971
-2
9’
-2
:El’
0
--
KM
1104c
N
-2 !?’
INSET
3t
26’
II
y
, 1000
,
METERS
EAST
I
I
IO’
162OE
FIG. 1.
Index
I
I
162O23’E
20’
map of Eniwetok
CHANNEL
Atoll.
Only
(1924) (76% yr-‘) to calculate a CaC08
production rate of 34,000 g CaCO,7 n~-2 yr-‘.
Odum and Odum (1955) made a more
comprehensive study of reef metabolism
across a windward interisland reef flat at
Eniwetok Atoll, also in the Marshall Islands.
Their estimate of reef calcification too was
incidental to the major thrust of their study,
and their proccdurc differed only slightly
from that of Sargent and Austin.
The
Odums estimated that corals covered 20%
of the Eniwetok reef flat and that the
average coral growth rate was 8 cm yr-1
(also from Mayor’s data).
Using thcsc
values, they then calculated an upward
growth of the reef of 1.6 cm yr-’ , or ( using
a coral bulk density of I.9 g cl+)
a production rate of CaCOa of 30,500 g CaC08
m2 Yr-” They also used their cstimatcs of
bulk density to rcvisc the production rate
of Sargent and Austin downward to 27,000
transects
II and III
I
I
24’
25’
are discussed
25’
here.
g CaC03 in2 yr-I, Both of the above estimates represent gross production and both
assume corals to bc the only significant
CaCO,s producers on the reef flats in qucstion. The Symbios Expedition to Eniwetok
(Johamms ct al. 1972) expanded on the
study by Odum and Odum (1955) and used
improved techniques; this work was done
during that trip. The primary survey arca
( Fig. 1, tr II) is adjacent to the Odurn and
Odum transect; a second transect was cstnblishcd 6 km northward, across another
stretch of reef flat (Fig. 1, tr III).
l’ROCl!xxJRE
The basic cxperimcntal design was similar
to that used in earlier investigations of reef
The chemical compoflat mc tnbolism.
sition of water crossing the reef is affected
by chemical reactions in the water column
and on the reef surface and by transfer pro-
108
S.
V.
ccsses across the air-sea interface. In an
environment as metabolically
active as a
coral reef, it can be assumed that biochemical reactions of the benthos are the dominan t chemical reactions. Observation by
Johannes ct al. (1972) on O2 consumption
by plankton vs. benthos support this assumption. If water crossing the reef mixes
thoroughly, then the product of conccntration change times water volume transport
across the reef equals the net rate at which
that component changes. Dividing
that
net rate by reef area gives the rate of change
per unit area. Let X equal the concentration
of some component:
AX me3 (m3 see-l) m-2 = AX m-2 see-l. (1)
In practice, it is convenient to express
the volume transport past a meter of reef
normal to the direction of flow and to
measure the distance which the water flows
in crossing the reef, yielding the same final
units :
AX II--~ (rn:%see-1 m-l) m-l = AX m-2 see-I. (2)
Our group as well as Odum and Odum
( 1955) observed that water flows from the
east across the Eniwctok windward
reef
flats almost unidirectionally.
The velocity
and volume transport of the water crossing
the reef vary as a function of tide and of
wave height. To observe the maximum
change in composition of seawater per unit
volume of water crossing the reef, we did
most of our sampling near periods of low
tides (both spring and neap). During low
tides water commonly crossed the entire
reef flat in less than an hour,
Dye released near the reef surface mixed
upward
through the water column to
the surface within about 10 m of its rclease position, indicating adcquatc vertical
mixing.
Samples taken during a number of low
tide periods over several weeks were usecl
to construct diurnal distributions to re,present an average day during May and June
1971. Metabolic processes arc assumed to
be indcpendcnt
of tidal state or volume
transport.
At tr II one team walked along the algal
ridge to the upstream end of a permanent
SMITH
transect lint, took water samples in 4-liter
Nalgene bottles at the “O-m station” (actually about 40 m behind the crest of the
algal ridge), and then measured the current
velocity with a small drogue or drift bottle
cithcr at the O-m station or preferably (to
minimize current variability
from surge)
about 100 m down the transect line. The
mean water depth at the current measurcmcnt site was also recorded so that volume
transport (velocity x depth) could bc calculated across a meter-wide strip of reef.
The’ sampling
encompassed periods of
volume transport ranging from 0.04 to 0.60
m 3 sccl fo,r each mctcr of reef front. A
second sampling team proceeded to the
downstream end of the transect line, 340 m
behind the O-m station, and collected water
near the surface and within a few dccimctcrs
of the bottom. Water was gcncrally < 0.5 m
deep at the upstream station and between
I.5 and 2 m deep at the downstream station.
At tr III collectors first sampled water
and measured velocity and depth about
280 m behind the algal ridge crest and then
waded 270 m upstream to sample water
crossing the ridge, Both tr III sites were
usually < 0.5 m deep when sampled.
On both transects, samples at cithcr end
were collected within a few minutes of one
another and returned to an air-conditioned
laboratory abroad the RV Alpha HeZix,
which was docked in the ICC of Muti Island
( Fig. 1). Three liters of each sample wcrc
filtered by gravity through Millipore filters
(0.8-p pore size). Unfiltered
water was
used for pH mcasuremcnts, and filtered
water was used for alkalinity determinations
( Culbcrson ct al. 1970). A Radiometer pH
meter (model PHM4d)
and combination
clectrodc were standardized to within 0.01
pH units with commercial buffers and read
to the nearest 0.001 pH units.
For alkalinity
dc terminations, 5 ml of
Titrisol
(a commercially
available, prestandardized IICl solution) diluted to 0.01
N and 20 ml of filtered scawatcr were used.
Particulate CaC03 trapped on the filters
was detcrmincd by Ca titration, according
to a slight modification of the EGTA tcchniquc described by Tsunogai et al. ( 1968).
Variability in the CO2 system at Eniwetok
ENIWETOK
REEF
FLAT
CO2
109
METABOLISM
day
ZII night
Atoll is near arralytical detection limits, so
all results discussed hcrc have been tcstcd
for statistical significance.
RESULTS
Transect descriptions
Transect II, near that of Odum and Odum
( 1955)) looks much like theirs, which they
described in detail. The following dcscription is concerned primarily with the calcifying organisms along our transect.
From the algal ridge crest, 40 m seaward
of our O-m station, to 160 m behind that
station, coralline algae are the dominant
calcifying organisms, Pavcmcnt of the reef
flat is cncrustcd by PoroMthon, while a turf
of Jania is abundant over the seaward half
of the arca. Resides these coralline algae,
scattcrcd corals, gastropods, and cchinodcrms arc the only other prominent calcif icrs .
The next 100 m corresponds to the zone
of small coral heads reported by Odum and
Oduni ( 1955). Porites microatolls are common, locally coalescing to form a false
pavement about 25 cm above the main
pavement.
The rcmaindcr of tr II, corresponding to
the zone of large heads described by Odum
and Odum (1955), is visually dominated by
Our
Millepora, Acroporq and Hdiopora.
downstream sampling locality was 340 m
behind the upstream station, Few conspicuous calcifying organisms inhabit the
coral rubble zone lagoonward of the downstream sampling locality.
The tr II sampling localities arc dcsignatcd 0, 340s (surface), and 340R (bottom).
Except for minor differences, tr III is
similar in general appcarancc to the turf
and algal pavement portion oE tr II. For
300 m lagoonward of the algal ridge crest,
the transect is a near-level pavcmcnt covercd with Porolithon and with a Janin turf.
.Both Porolithon and the ]a& seem more
luxuriant on tr III than on tr II, Foraminifcra (cspccially Cdcarina) and small gastropods are very abundant in the turf of
tr III. The tr III algal ridge is more rugged
than at tr II. Sampling localities wcrc about
10 m behind the algal ridge (0 m) and
0
0
q
:
0
0
0
FK. 2. Scatter diagram showing offshore mean
alkalinity
nncl pH as well as the alkalinity
and pII
Note the
values rccordcd
on the two transects.
clcnr division bctwccn day and night values as a
function of pH but not of alkalinity.
270 m downs,tream of that station (270 m
station).
Transect
nlknlinity
and pH data
Figure 2 and Table 1 summarize the pH
and alkalinity data for the two transects.
The figure clearly demonstrates that the ~1-1
of reef water samples increases over offshore
water during the day and dccrcascs at
night, Alkalinity shows no such consistent
day vs. night or reef vs. offshore variation.
The diurnal pI1 variation is consistent with
the observations of Schmalz and Swanson
(1969), and a near-cons,tant total alkalinity
with diurnally varying pI1 would yield the
variation in C,aC& saturation reported by
them. Omdum and Odum (1955) found the
same gcncral pattern in pH.
More important to this study arc the
changes in C:Oa content of water crossing
the reef. If the partial prcssurc of CO2
in the water differs from that in the ovcrlying air, then gas exchange across the
110
Table 1.
S.
V.
SMITH
Mean, stnndarcl deviation, and number of observations for the parameters measured on the
two transects and offshore
Total Alkalinity
Suspended C&O3
PH
bdm3)
2.292+0.020 (17)
2.294'0.025
(7)
2.286+0.014 (17)
2.291kO.026 (7)
2.233+0.019 (11)
2.290+0.025 (6)
8.31iO.02 (19)
8.28tO.01 (8)
8.34+0.04 (19)
8.2720.02 (8)
8.35kO.04 (13)
8.27kO.02 (7)
20+13 (21)
2.294+0.017 (12)
2.304+0.013 (5)
2.281+0.022 (8)
2,303+0.013 (5)
8.31kO.03 (12)
8.2720.02 (5)
8.36iO.06 (8)
8.25AO.03 (5)
2.290+0.023 (11)
8.30+0.02 (13)
(mcq/liter)
Transect II
0 m (day)
0 m (night)
340 m surEace (clay)
340 m surface (night)
340 m bottom (clay)
340 m bottom (night)
22213 (18)
27216 (14)
Transect III
0 m (day)
0 m (night)
270 m (clay)
270 m (night)
OEfshore
air-sea intcrfacc is likely. Solution or prccipitation of C,aC10:3will raise or lower the
CO2 content of the water, as will oxidation
or reduction of organic carbon.
The primary difficulty
with the CO2
system as a record of community mctabolism is its cxtrcmc complexity.
Yet, as
discussed by Park ( 1969) and others, mcasurcmcnt of two or more parameters in the
CO2 system is sufficient to partition the
CO2 in scawatcr into its constituent species
and to differentiate
changes into those
arising from ClaC03 precipitation or solution
and those due to organic carbon systhcsis
or utilization.
Park’s ( 1969) discussion of
the USC of pH and alkalinity as the two
master variables requires clarification.
Total alkalinity
rather than carbonate
alkalinity is the most readily usable record
of C,aC,03 precipitation
or solution. This
fact is most easily appreciated by realizing
(see Edmond 1970) that a pI1 shift in the
abscncc of C&O:, precipitation or solution
changes the partitioning
of carbonic acid
species to affect the carbonate alkalinity
without altering the total alkalinity.
Also,
carbonate alkalinity rather than total alkalinity must bc used in calculating the
total CO2 content of scawatcr. Carbonate
alkalinity can bc calculated from the total
alkalinity, the pH, and the total boron content of seawater (assumcd constant for a
23flO (10)
15211 (8)
U3+21 (10)
constant salinity).
Park’s discussion did
not spell out thcsc distinctions of usage bctwcen carbonate alkalinity
and total alkalinity, but Edmond pointed out that only
recently has the analytical precision with
which alkalinity can bc measured warranted
the practical distinction.
A third point is that differentiating
COZ
changes into those due to precipitationsolution and those due to oxidation-rcduction is valid only in the absence of C;OZ
gas transfer to or from the water. Park
( 1968, 1969) has b ecn primarily conccrncd
with the CO2 system of the deep ocean
where an assumption of no gas transfer is
likely to be valid. But thcrc is no a priori
basis for making such an assumption for
the shallow and turbulent water of a coral
reef flat. Thcreforc, the problem of gas
exchange is considcrcd hcrc.
Various workers
(e.g. Edmond
and
Gieskcs 1970; Takahashi et al. 1970; Wangersky 1972) have pointed out that USC of
carbonic acid apparent dissociation constants in seawater does not always yield
satisfactory results of Cm02speciation. Their
arguments apply primarily to samples with
widely varying pII, a problem not cncountcrcd in this study (Fig. 2). And their
arguments apply to studies conccrncd
primarily with accuracy. Precision, rather
than accuracy, is the limiting
analytical
ENIWETOK
REEF
FLAT
consideration
of this study, because the
diffcrenccs between pairs of samples providc the record of metabolic changes. Precision should suffer little from shortcomings
which ,thcsc authors attribute to apparent
dissociation constants.
The obvious advantage of the COb system
over C’a as a record of calcification is prccision. Calcium can be dctcrmined routinely
to a precision standard deviation of about
0.02 mcq liter -l in scaw’atcr (Tsunogai et
al. 1968 ) , but alkalinity can bc measured
to a precision s,tandard deviation of about
0.004 meg liter-’ (Culbcrson et al. 1970)-a
fivefold
advantage to the CO2 system.
Because calcification was the parameter of
primary intcrcst here, this advantage was
dcemcd sufficient reason to USC the COO
system primarily as a record of reef flat calcification and secondarily to describe other
changes in the CO2 system there.
At least three replicates were used for
all but a few total alkalinity determinations.
The precision standard deviation obtained
for 133 sets of rcplicatc analyses was 0.0034
mcq liter-*. A conservative estimate of the
accuracy of the method can ‘also bc presentcd. If the water arriving at the algal
ridge is invariant in alkalinity, then daily
variation observed is due only to random
errors about some mean. The mean alkalinity for 43 algal ridge samples is 2.295
mcq liter-’ (SD, 0.016 mcq liter-’ ), Scparate bottles of water from the reef front
were analyzed in single batches on four
occasions. A mean alkalinity standard deviation of 0.0028 mcq liter-’ was obtained for
these batches. Because #this within-batch
standard deviation is small compared to the
accuracy standard deviation, it appears that
variations in alkalinity dctcrminations arise
from batch-to-batch diffcrcnces rather than
from bottle-to-bottle
diffcrcnccs within a
batch. This situation is fortunate because
it indicates that the ability to distinguish
bctwccn alkalinity
samples in the same
batch ( or sampling run across the reef flat)
is limited by the precision of the method
and not by bottle-to-bottle
differcnccs.
Similar cart was cxcrciscd with pI1 mca( or more ) analyses
surcmcnts. Triplicate
CO2
111
METABOLISM
were pcrformcd on most samples, and a precision standard deviation of 0.0035 pI1 units
was calculated for 151 sets 0E replicate
analyses. The pH values arc reported here
to 0.01 pH unit, so an error of 0.005 pH
units has been assumed for an individual
For 45 samples, the mean
dctcrmination.
pH of the reef front was 8.30 ( SD, 0.03 pI1
units ), establishing a conservative estimate
of the apparent accuracy of the pII detcrminations.
Total CO2
Clarbonatc alkalinity (GA) and then the
total dissolved CO2 content of se’awatcr
( 8C02) can be calculated from pII and
total alkalinity
(Th).
As discussed by
Skirrow ( 1965 ) , Lyman’s apparent dissociation constants for carbonic acid ( K’T,1 and
K’z) and first apparent dissociation constant
for boric acid (K’,]) arc used for these
calculations ( T = 28” C and chlorinity =
19%, ) . Furthcrmorc, let us assume that the
total boron content of seawater (I: B ) remains constant and that hydrogen ion activity ( arI) equals lo-pn.
CA = TA - (K’,j Z B) (&
+ an) -l.
14CO2 = CA]1 + Z;(‘&Z,~)-~ + arr(&)-“1
]l+ 2K’&rr)-I]-‘*
(3)
x
(4)
Mean 8C02 for Eniwctok water is 2.0
meq liter-I, with only slight deviations from
that value. All subscqucnt discussion is
conccrncd with A8C02. Figure 3 illustratcs aXCOz for water crossing the two
transects during
the day and during
the night. The communities of both transects clepletc the CO2 during the day and
increase it during the night, a pattern consis tent with net utilization of carbon during
the day and net carbon relcasc at night.
Both communities show a gcncral tendency
toward a midday carbon fixation peak but
no clear nighttime pattern. Although both
communities have a roughly similar spread
of nighttime C:Oa incrcascs, the algal turf
(tr III) is markedly more active than the
coral-algal transect (tr II) in daytime CO:!
uptake. A more dctailcd interpretation
of
these data follows.
112
S.
V.
SMITH
0
FIG. 4. Histogram of Pcoz values for reef samplcs. Virtually
all samples have a lower Pcoa than
the atmospheric value, a.
FIG. 3. Rate of change in total CO, vs. time of
day. ZCOz is deplctcd in transect waters dukg
the day (unshaded portion of the diagram)
ancl
enriched at night (shaded).
co2 partial
pressure
Gas exchange across the air-sea interface
is driven by the diffcrencc in gas partial
pressure on either side of that interface and
by the turbulcncc at that interface. Ocean
atmosphere pco, rarely dcviatcs by more
than a few ppm (p atm) from 315 ppm,
and oceanic Pea, can be calculated according to equation 38 from Skirrow ( 1965)
(the Henry’s Law coefficient
for CO2
is a):
Pco, = CA~r[K’ma{l+
2K’&&1}]-1.
(5)
Such calculations with the Eniwctok pH
and alkalinity data yield the histogram of
Poo2 values shown in I?ig. 4; Eniwetok reef
waters have a Pco, deficit both before and
after the water crosses the reef flat, so (202
should constantly cntcr the water. Schmalz
and Swanson (1969) report similar, gcn-
erally below-atmospheric
reef water values
of ho, at Eniwctok.
Figure 5 is a plot of the average Pcos of
water at either end of the transects vs.
A8c02
of water crossing the reef. Invasion
rate constants of COZ, mcasurcd by Sugiura
et al. ( 1963) to lie bctwecn 0.001 and 0.007
~molc md2 see-r ppm-’ under a variety
of conditions of turbulence, can be used as
rough indicators of the importance of CO2
exchange to the overall pattern in A8c02
observed.
Let the superscript n denote atmospheric
pco2 ( -315 ppm ) and ZL,bc the mean Pco,,
of water crossing the reef during a particular sampling period. The cxpccted gas
invasion rate per unit #arca (R) for this
sampling period can bc calculated from the
invasion 1ate ,constant ( k) and these two
values :
R pmolcs rn-:! see-’ = 7c(p,oan- Pcozw). (6)
The lint with a gcntlc negative slope on
Fig. 5 represents the gas invasion to bc
expected if the appropriate invasion rate
constant is 0.007; g,as invasion cvcn with
this conservative constant is slight relative
to the total changes observed. If the lower
ENIWETOK
REEF
FLAT
:.-..“..:.:
0-~-_
‘..
-;-r ~~
CO2
113
METABOLISM
... . :. : .. l ., ‘f i: .j :. 1::: 1: .j: y
,. .:. y ., ,:.,:. ‘,’
“,.: ,::,,.::
:.
: .‘.‘.’ :;,
..‘,
.; j;:.:y
:.
;;.,.
:
.. .. :::..
..
.:
“‘.,,,’ i ::: $!‘:
‘j ‘;‘:‘. ‘.:“‘;:‘a”,“:::
:
&‘,
; 1; .. ‘1 ,, .; f.,:.:
: ‘, ,:: ,:.
: ::::
;:.
,I., .,,,:.:
..’ ; ,,., :.<..:
.. ; ,. : :. .’ :
,’
:.:*:.,
,, ,:: @ .. ;;;:
‘:‘I.‘:
::..:y
.. ” .,.
.,..
.. :. : :, : :.j: ,’ .‘. : .::
:,
,: 1: j::.
~, ,:, :: 1: ,.
;I
.’
....
: “’
0
.
00
00.
00
-1
.
g
B”
.
0
.
-3
0
.
-2
LI
,"
-I- -r
Ic
r(^
. . . ..'. ,',' :: ,:: ', >. .:,. ':
:,i .~~~~~~'~"~~~~~~:"~~:,'.l~',~'~.;,,~~.~; 2
"
8
,
IT
C.
a
I
-‘Ye
:
0
‘.
260’
hm)
I
280
I
300
320
FIG. 5. Plot of mean Pco2 along transects vs.
the total CO, change observecl on that transect.
The lint with a gcntlc negative slope clenotcs the
probable maximum AXO,
attributable
to gas exchange as a function of low reef water values of
Pco2*
invasion rate constant measured by Sugiura
et al. is used, then the slope of the line
would be $$ the illustrated slope. They
pointed out that other workers have rcportccl even lower C,Oz exchange rates, so
most Eniwctok
samples probably dcrivc
< 10% and pcrh,aps < 1% of their CO2
characteristics through gas cxchangc. In
subsequent sections, I will thcreforc ignore
gas cxchangc. An explicit gas-cxchangc
correction cannot bc macle, because the best
estimate for the appropriate invasion rate
constant under the turbulence conditions
prevailing is not known.
Calcification
Figure 6 illustrates rates of change in
total alkalinity of water crossing the two
reef flat transects, cxprcsscd per square
meter of reef floor. Each alkalinity change
from paired ups trcam and downstream
samples (meq m-” ) has been multiplied
by volume transport per unit length of reef
front (1~~~set-1 m-l ) ancl divided by transect length (m) to yield a value for the rate
of alkalinity change per unit arca (mcq
in-2 see-L) ,
Statistical analyses by t tests demons tratc
that most combinations of day vs. night and
::.
,‘+,
:.
*
:“;I: ;,,
0
240
Go2
._
5
bn
E
3
-40
1
I
.' ::tr
II
1: ; :< :.
':
s
':.I
,, ,,,.'.y,':'.:'"",. 100 ul
: ,.. . :,..:., ',,.,
,' : F
: : :: ,,,:" j . .
N
/.: ,:i ;I.': surf&f,~..
.:
I~
.: ". :
:., 13ottom
0'
'
m
... ... ., ...
.::,
.
.
-3
N
0
2
4
Cl
0
-1.
; :,
: ,' ', :
v.
,.: j: tr
0
0
_ 3 r _,
08
i2
,
:
ic,
Time
,’
‘: .’ ‘: ‘: :,
: ‘, : .,:.:.,
.. 0
:‘:
“. j..:i.:;.
:
,‘:.:‘,‘,
.,. . . .
: '..,:
:; ., .,. .,g., ::: .::::;y:
,' ,, : .; f .?,::':.'.
.T,...
II'y.',;'.:"'.
1: ,'.,
c
.;:0
;
r;]
VI
::
u"
,.... .. :.... .. :. .:: : : :, 100
: : .: .,.:..: : : :;.j;::
.. .,," ',:,'::I.',:
':'. .'.'."...:.
.;,', ; .. 1::: F:
:' :' ':. : : :'I
,:.,.:
., : .. jj;::,.: :,
::'C; '.i.3,.~~:.,.:~.~:;._:.::..~;.:~
“i ""
20
24
04
-2
00
, _
x--‘-7rT.
‘. ,“.’
..
‘5,:;. :.‘;:“,’ :;.
of
day
FIG. G. Rate of change of total alkalinity
(and
cquivalcnt
calcification
rate) vs. time of clay. Alkalinity depletion rate is about the same on both
transects, both day (unshaded) and night (shaclcd).
tr II (top and bottom) vs. tr III alkalinity
changes do not differ significantly from one
another but do differ significantly
from 0
( at P = 0.1). The record is clearly one of
alkalinity dcplction. Neither salinity changes
( as mcasurcd with a conductivity salinometcr; the mean salinity is 34.52,) nor nutricnt changes (as measured by K. Webb
and M. Pilson, personal communication)
are sufficiently large to account for a significant fraction of the observed changes in
alkalinity.
Virtually all of the change obscrvcd apparently results from calcification.
Total alkalinity should bc dcprcsscd by 2
mcq for each mmolc (100 mg) of CaCOz
prccipitatcd.
The mean alkalinity depression, day and night, across the two transects is 2.5 ,zcq m2 see-’ ( SE = 0.4), corresponding to an annual net calcification
rate of 4,000 g CaC,On m-2 yr-l ( SE = 640).
Production and respiration
Oxidation and reduction of organic carbon
compounds to yield or consume COz can
bc assumed to bc primarily the result of
community
respiration and primary pro-
.
114
S.
V.
SMITII
Roth
plots arc gcncrally similar to the
plots illustrated in Fig. 3. The
main difference is the abscncc of a pronounccd midday deplction peak of COz at
tr II on Fig. 7. A scale of organic carbon
production
and consumption
has been
added to the right side of Fig. 7.
Although the daytime values of tr II
differ significantly
(P = 0.1) from the daytime values of tr III, the nighttime values
of the two transects do not differ significantly from one another. Thcrcfore
all
nighttime values have been pooled to yield
one estimate of reef flat respiration, and
daytime net production cstimatcs of the two
transects are reported scparatcly.
Transect II, visually dominated by a mixture of corals and nlgac, has a daytime net
production rate of 0.25 g C m-2 hr-l (SE =
0.03). Transect III, dominated by algae,
has a daytime net production rate of 0.72 g
C m-2 hr-1 ( SE = 0.21). The pronounced
midday production peak of tr III accounts
for the relatively high standard error about
the mean value, The nighttime respiration
rate for the two transects is 0.12 g c’ me2 hr-1
(SE = 0.03).
If the daytime respiration rate equals
the nighttime rate, then the daytime hourly
gross production rate is the sum of the daytime hourly net production rate plus the
nighttime hourly respiration rate. If one assumes 12 hr of daylight and 12 hr of dark,
then the 24-hr gross production to rcspiration ratio is gross production divided by
twice the respiration. Transect II shows a
gross production
to respiration ratio of
about 1.5, and this ratio is about 3.5 on tr
III; both transects apparently produce more
organic carbon than they consume.
AZ$cOz”
Time
of
day
FIG. 7. Rate of change in noncalcification
CO,
(ancl cquivalcnt
organic carbon production
and
respiration
rate) vs. time of clay. Daytime
production rate (unshnclccl areas) is greater on tr
III than II, but nighttime respiration rates (shad&l)
on the two transects arc about equal.
duction in the shallow, highly productive
waters of the reef flat. The following discussion of Eniwetok production and rcspiration is prcsentcd for the sake of a completc analysis of the GOa data. Smith and
Marsh (in preparation)
discuss certain aspects of thcsc data in dc tail.
Let the superscripts T, g, c, and p clesignate CO:! components attributable
to
total, gas exchange, calcification-solution,
and production-respiration
reactions, rcspcctivcly.
Particulate
A8CozT
= A8C020
+ A8c02”
+ A%&?
(8)
~W202~’ is known ( Fig. 3); AZCO# has
been assumed on sthc basis of the preceding
discussion to bc negligible;
and AI)CO,”
equals half the change in total alkalinity
(Fig. 6) for each sample. Consequently
ASC:O,~~can be estimated. Fig. 7 is a plot
of AxC:Onz’ vs. time of clay for each transect.
CaCOR
In addition to the dissolved CO2 flux
results rcportcd above, it is useful to make
some cstimatcs of the transfer of particulate
Suspcndcd CaC,Os immcdia tcly
CaC03.
windward of Eniwctok and across the reef
flat avcragcs about 20 mg CaC03 m-3,
similar to open tropical Pacific Ocean values
reported elscwhcre ( Smith et al. 1971). NO
significant
change in suspended CaCOs
ENIWETOK
REEF
FLAT
occurred as water crossed the windward
reef flat (Table 1). The following calculation suggests that gain or loss of CaC03
as suspended load was of minor importance
during our stay at Eniwetok.
During one
g-day period a continual record of current
speed and water depth on tr II yicldcd an
average volume transport of 0.8 m3 set-l
m-1 (J, Maragos and R. Cxlutter, unpublished).
Both transects are about 300 m
long, and the change ( cithcr gain or loss)
of CaCOa in water crossing the reef is apparently less than 10 mg m-3. Substituting
these values into equation 2 yields suspcndcd CaCO:$ flux ( either gain or loss ) of
< 800 g CaC03 n--2 yr-l.. Apparently, cithcr
gain or loss of suspended C,aC’O:%during
sea conditions such as prevailed amount to
less than 20% of the amount of CaC03
precipitated on the reef flat.
Potholes on the algal ridge accumulate
calcareous rubble apparently washed in by
the surf from the forerecf slope. R. Johannes
( personal communication)
provided information by which the role of such rubble
input to the CaC03 buclgct of the reef flat
can bc cvaluatcd. One such pothole 1 m
long parallel to the reef front accumulated
70 g CaCO:$ day-l over two 4-day periods
and 170 g clay-l over a g-day period, The
high value was anomalous, bccausc it followed blasting on the forcrccf slope immediately upstream of the pothole. Nonctheless, the high value serves to place a
likely upper limit on introduction
of matcrial from seaward of the algal ridge during
normal conditions.
Input of that amount
across a strip of reef 1 m wide and 300 m
long is equivalent to an avcragc input of
about 200 g CaCO,3 n1-2 yr-l, or only about
5% of the rate of CaC:& production on the
reef flat.
IXXXJSSION
The CO2 system as a methodology for
marine metuholic studies
Ryther (1956) pointed out that organic
carbon production in aquatic cnvironmcnts
might well be measured by changes in dissolved CO2 were it not for certain umder-
CO2
METABOLISM
115
lying disadvantages.
IIc cited the complcxity of the marine C#Oa buffer system
as the major disadvantage
and further
stated that any environment undergoing calcification would rcndcr CO2 useless as a
record of aquatic organic carbon production.
Workers using the CO2 system as a
record of aquatic metabolic processes have
since over&me each of thcsc problems. In
gcncral, they have done so by dealing with
situations where they felt they could ignore
calcification.
For example, Verduin ( 1956),
Reyers ( 1963)) and Hufford
( 1965) all
used empirically
determined relationships
between pH and 8C02 as records of organic
carbon production
and respiration.
Tc,al
ancl Kanwisher (1966) monitored Pco, and
estimated SC,0s2 from that. All have tither
knowingly or otherwise assumed that total
alkalinity remains constant (i.c. no calcification ) . Park ct al. ( 1958 ) used an approach analogous to the one taken here;
they measured both pH and alkalinity
( carbonate rather than total) and calculatcd X02.
All of the above workers have
cstimatcd ~$02 changes and have (implicitly) ruled out calcification and solution
They
as significant contributors .to A8C02.
have also assumed that CO2 exchange
across the air-sc.a interface is ncgligiblc.
Thcrcforc, they have been left with a number from which they could cstimatc organic
carbon production and respiration.
In at least two s tudics, Rroccker and
Takahashi ( 1966) and Kinscy (in press),
alkalinity changes have been used to calculate calcification rate. The former used
carbonate alkalinity,
and the latter used
total alkalinity.
Thus, all of the above workers have
gotten around the problems raised by
Ryther ( 1956) and have used the COz
system to record single metabolic processes
(cithcr organic carbon production and respiration or calcification)
in aquatic environmcnts.
Park ( 1968 ) and Smith ( 1971) have used
pII and 02 data to partition oceanic pH
changes into those due to organic carbon
oxidation and those due to C’aC;03 solution.
Those studies arc rclcvant in that they are
116
S.
V.
SMITII
0.1. By comparison, Kahn and IIclfrich
cxamplcs of describing two C02-altering
(1957) suggested .that the correction for
proccsscs simultaneously.
The contribution
of my investigation to 02 exchange appropriate for the reef flat
cnvironmcnt
they studied in IIawaii was
the methodology
of marine metabolic
about 0.2, a value comparable
to the
studies is the implementation of a procedure
ASCO,“: A8C:OzP ratios listed above.
irnplicd in all of the above studies-that
A second possible disadvantage of the
the CO2 system can be used as a simultaneous record of both organic carbon pro- CO2 system is the high CO2 concentration
as compared to O2 concentration.
At Eniduction ancl calcification.
Besides the dual
return of information,
the proccdurc is wctok, XC02 is about 2 mmoles liter ’ and
02 concentration is about 0.2 mmolcs liter-’
satisfactory for other reasons.
or 10% of the CO2 concentration.
To a
Both pH and alkalinity can bc measured
first approximation, the molar ratio of mctaprecisely with a pH meter and very little
clsc. Although the marinc CO2 system is a bolic 02 transfer to metabolic CO2 transfer
complex and largely disequilibrium
system, is about -1 (e.g. Sargent ancl Austin 1949,
the equilibrium
assumptions rcquircd for 1954; Johanncs et al. 1972); so for comthe above proccdurc involve only the dis- parable resolution of organic carbon transsociation of carbonic acid into I-ICO:s- and fcr, CO2 must bc measured with 10 times
the rclntive precision of 02.
C0,j2--proccsscs
that arc cxtrcmcly rapid
( Kern 1960). A final, and perhaps crucial,
CO2 and organic carbon transfer
characteristic of the CD2 system as a record
of marine metabolic proccsscs is the slugThe organic carbon aspect of the CO:!
gishncss of CO2 exchange across the air-sea
system is covered only briefly hcrc. Both
intcrfacc. The work of Sugiura et al. (1963) transects arc highly procluctivc, and aphas already been discussed in this context.
parently both communities produce more
I,ess quantitative but also useful is the in- organic carbon th,an they consume. Tranvcstigation by Kanwisher (1963), suggesting
sect III, the algal community, is considerthat -CO2 diffusion and bubble transfer
ably more productive than tr II, the coralacross the air-sea interface proceed tens to algal community, and has a much higher
hundreds of times more slowly than does gross production to respiration ratio. This
O2 transfer. A graphic illustration
of the observation suggests that the major organic
slow rate of CO2 transfer is Keeling’s (1968) carbon producers on a reef flat arc not inmap showing regional P(:o, anomalies in the timately associated with the corals. Rather,
surface waters of the world’s oceans of up the prcscnce of the corals actually appears
to gre#ater than 30%, although open ocean to lower the capacity for organic carbon
PO, anomalies apparently only rarely, tcm- production, as well as the gross production
and locally exceed about 5% to respiration ratio, on the reef flat.
pornrily,
( Richards 1965).
Finally, the Eniwctok reef flats support
Two possibly important
disaclvantagcs
the observation of others (e.g. Odum 1956;
also need to bc mcntioncd. Prccisc USC of Odum et al. 1959) that high production is
the COz system as a record of organic
probably characteristic of various commllcarbon production and respiration rcquircs
nitics bcsidcs coral reefs in shallow flowing
that a correction for CaC’O:s precipitation
water.
or solution bc made. If handled as here,
C&OR hutlget
that correction is straightforward.
Furthcrmore, its magnitude is similar to the corThe impetus to this investigation was the
rcction for O2 diffusion to be expected if dcsirc for direct estimates of reef community
Previous cstimatcs of gross
calcification.
that gas is used insteacl of CO2. The ratio
C’aCO:l production on coral reefs have used
of AZ&Co12c:A8C02P at night on the two
transects is -0.4; the daytime ratio on tl standing crop and turnover data, as disII is 0.2, and on tr III the daytime ratio is cussed by C11,nvc ct al. ( 1972). Gross pro-
ENIWETOK
REEF
FLAT
duction, in their terminology, is the sum of
the proportion of cover times the turnover
for each calcarcous organism. The procedure is conceptually simple but is both
tedious and inaccurate in practice. Community calcification, as recorded by alkalinity changes, mcasurcs a charactcrismtic
that differs somewhat in concept from gross
ClaC03 production. Such a proccdurc mcasurcs gross production plus inorganic precipitation
(such as ccmcntation)
minus
solution. The following considerations suggcst that the two sets of values do not really
differ greatly from one another in this
.
I instance
L
2.
Buddemcier ct al. (in press) have dcmonstrated that virtually no calcareous material
other than a few ccntimcters of algal vcnccr
an d scattered coral thickets have accumulatcd on the Eniwetok reef flat over the last
several thousand years. Nor is there evidence of significant inor&anic precipitation
in the void spaces of the young material
which is present on the reef flat. Conscquently, inorganic precipitation can bc ruled
out as a significant contributor to the net
calcification
obscrvcd.
Since Eniwctok
waters are apparently supersaturated with
rcspcct to most C;aC0,3 phases present
( Schmalz and Swanson 1969 ) , inorganic
solution is likely to bc ncgligiblc.
Two published estimates suggest that biochemical solution is minor as well, Bardach
( 1961) estimated that fishes browsing on
the calcareous substrata of Bermudian reefs
ingest and redeposit about 200 g C,aCO:!
m-2 yr-‘, Tl WC fishes are likely to dissolve
only a small fraction of the material they
ingest. Ncumamr ( 1966) reported that a
100% cover of boring sponge could erode
up
to 20,000 g C:aCOR rnd2 yr-’ and dissolve
perhaps 10% of the crodcd material. Boring
sponges cover muc11 less than 100% oE thr:
Eniwctok reef flat, so they arc unlikely to
dissolve as much as 1,000 g CaC,O:{ m-” yr-‘.
Studies of alkalinity depletion at Eniwetok
yicldcd a calcification rate of 4,000 g CaC03
rn2 yr-I, The total effect of the above processes seems likely .to amount to < 1,000 g
CaC:Ols m2 yr-I-, This possible cffcct is sufficicntly close to the standard error of the
CO2
METAROLISM
117
calcification rate (640) that the effect can
bc ignored; apparently no significant differcnce cxis ts #atEniwetok bctwccn net calcification and gross CaCO:( production.
It was argued earlier that little loss of
particulate C:aCIORfrorn the reef flat occurs
during normal sea conditions, so net calcification (gross production)
approximates
net production ,much of the time. If the reef
sediment and fra,mework being produced
have a porosity of 50% and if the material.
remains where it is produced, then 4,000 g
CaC:OR m-2 yr-I is sufficient for 3 mm yr -I
upward reef growth. Yet thcrc has been
neither a significant change in sea level nor
a significant accumulation of material on
the reef flat over the last 4,000 years
( Buddemcicr c,t al., in press). Therefore,
the reef flat apparently loses all the calcareous material that is produced there.
The calcarcous material accumulating lagoonward is the probable sink for most of
it. It is likely that sediment transport occurs almost cxclusivcly during periods of
intcnsc wave action. Stoddart (1971) has
summarized stlrdics demonstrating that cxtcnsivc reef destruction and scdimcnt rclocation occurs during storms,
It is useful to consider the relation of
sea level changes to calcification rate over
other periods as well. B. Chrtter and I
were able to locate ,a specific large coral
head appearing in an air photograph in the
Odum and O,clum (1955) paper, so the tr
II reef flat has apparently not been swept
clean of all of its cxoess calcarcous products
for at least 20 years. On the other hand, the
fragile algal turf present on both transects
is probably removed much more frcqucntly
than that. For example, Doty ( 1971) has
dcmonstratcd that the standing crop of
algae on an Hawaiian reef fl#at reflects to a
great cxtcnt the degree of algal removal by
waves over ,the several weeks preceding the
mcasurcmcnts.
Data provided by S. 13. I-licks dcmonstratc that although the annual mc8an sea
level of Eniwctok oscillated by as much a
10 cm yr-’ bctwecn 1952 and 1970, thcrc
was no significant
net change in mean
sea lcvcl over that period. Therefore, tr II,
118
S. V.
which has apparently retained much of its
products over that period, m,ay have shoaled
by up to 5 cm (3 mm yr-’ x I8 year) relative
to mean sea Icvcl. During individual
periods of 1 to 6 years over that time span the
reef flat may have either shoaled or deepencd by as much as 15 cm, It is likely that
no net accumulation has occurred on tr III.
Thus, net production over the past 20 years
has probably been near gross production
on tr II and near 0 on tr III.
By contrast, sea level before about 7,000
years ago apparently rose by more than 10
mm yr-l (Milliman
and Emery 1968; and
others ). Such a rapid rise could not have
been matched by the rate of calcification of
the prcscnt reef flat community, Three possible interpretations
for this situation can
be imagined. The calcifica.tion of the reef
flat community may not have been sufficient to maintain the reef flat at sea lcvcl.
Commmlity structure may have been similar
to now, but organisms may have calcified
more rapidly than they do now. Or the
relative and absolute abundance of the reef
flat biota may have been shifted to favor
the more rapidly calcifying reef organisms.
,4gain, more data arc nccdcd to rcsolvc this
question. However, observations by Buddcmcicr ct al. (in press) suggest that the
prcscn t cnvironmcntal
sc t ting, and hence
the present community struoture, is less
than 4,000 years old.
The data on calcification rate gathcrcd
during this study are dramatic,ally lower
than the estimate made by Odum and
Odum ( 1955) f or a transect near and apparently similar to tr II. Chavc c-t al. (1972)
rcviscd the Odum figure downward from
3 x 10” to 7 x IO” g CaC,Ox m-2 yr-l by
using a diffcrcnt intcrprctation
of Mayor’s
( 1924) growth data than had the Odnms.
Data on coral standing crop gathered by
R. Kinzic (unpublished)
suggest that the
Odum estimate of 20% coral cover may have
also been somewhat high. Such corrections
would bring the Odum estimate to close
agreement with the value cstimatcd here.
This initial discrepancy and its resolution
demonstrate the large uncertainties inherent
SMITII
in the standing crop and turnover approach
to estimating CaCO:{ production
of the
community, Chavc et al. (1972) also conccivcd a simplified hypothetical
reef flat
community with gross production rate of
3,000 g CaCOx m-2 yr-I.
Another discrepancy bctwccn the results
of my study and the conclusions of Odum
and Odum (1955) and Sargent and Austin
(1949, 1954) 1its in their assumption that
corals are the major producers of CaCO:%
on a reef flat such as tr II. The oalcification
rate at tr III, with virtually no corals, is
similar to that of tr II, which has corals.
Just as inconspicous organisms may be
important contributors to organic carbon
flow in a community, they may also contribute gre’atly to community calcification,
Such a conclusion agrees with the suggestion of Chavc et al. (1972) that a wide
variety of organisms exhibit similar rates
of potential CaCOs production in spite of
considerable variation in size.
And finally, my observation that daytime
and nighttime claIcification rates at Eniwctok clo not differ greatly from one another
contrasts with the observations of Goreau
( 1961) and others that many calcifying
organisms apparently calcify much more
slowly in the dark than in the light. Various
possibilities might explain this discrepancy.
It is possible that the calcification charactcris tics of organisms in flowing water ( such
as the windward
reef fiat at Eniwetok)
differ from the characteristics
of those
same organisms in still water (such as
Gorcau’s bell jars or some natural reef
situations ) , A respiration-rclatcd
buildup
of CO2 in still water could account for such
a response. Also, the possibility cannot bc
discomltcd
that inconspicuous
organisms
whose calcification characteristics have not
been well. investigated may differ significantly from the more prominent calcificrs
that have been studied. C’crtainly, Gorcau
( 1961) rcportccl on some organisms with
roughly similar day and night calcification
Some diffcrcnccs in charcharacteristics.
acteristics of day vs. night calcification at
Eniwctok may be lost in the scatter of the
data.
ENIWETOK
REEF
FLAT
CONCLUSIONS
A major contribution of this investigation
is the successful USC of the marine CO2
system to monitor organic carbon production, respiration, and calcification
in the
marinc environment.
Previous studies of
marine community CO2 metabolism have
dealt cithcr with organic carbon productionrespiration or with calcification,
This study
has combined established theoretical information with newly av,ailablc analytical
mcthoclology of high precision to monitor
these processes simultaneously.
Although
the tcchniquc
applied to flowing water
respiromctry is demanding on prcscnt capabilitics of resolution, it should bc easily applicable in incubation chambers or in natural water, low-flow rate situations.
General agreement bctwcen this production-respiration
study and the results
of previous investigations
inspires confidence in such C:02 metabolism studies.
The reef flat at Eniwetok
is a highly
productive
cnvironmcnt
which produces
slightly more organic carbon than it consumes. The cxtrcmc production is not confined to communities visually dominated
by corals; an algal turf community nearly
devoid of corals proved both to bc more
productive and to show a higher gross production to respiration ratio than a nearby
coral-algal community in a similar physical
setting.
The calcification rate of the reef flat community at Eniwetok is considerably lower
than had previously been cstimatcd thcrc,
but is well in agrclcmcnt with gross production rates of CaC03 cithcr cstimatcd or
mclasurcd in a variety of reef cnvironmcnts.
Two distinctive reef flat communi tics calcify at about the same rate, suggesting that
physical-chemical
setting rather than biological composition may be the most important factor controlling the calcification
rates of marine communities.
This suggestion is supported by my observation
( Smith 1972) that three temperate-wa tcr,
hard-bottom, shallow benthic communities
exhibited calcification rates similar to one
another despite considcrablc
diffcrcnccs
in dominant biota. On the other hand,
CO2 METAl30LISM
119
within
a particular
physical setting the
ability of a community to retain CaCOs is
surely a function of its biological composition (e.g. Ginsburg and Lowcnstam 1958).
The present virtually unchanging sea level
allows little or no vertical accrcti.on of the
rclef flat, so all of the calcarcous products
of that environment
arc eventually
removed.
Other conditions
of sea level
changes might demand adaptNation of the
co,mmunity to cnhancc CaCO:$ retention as
well as production.
Finally, increased knowlcdgc about the
link between organic carbon production and
calcification
might eventually
allow the
geological record to provide quantitative
historical information on rates of biological
production.
BAIIDACII, J. E. 19,Gl. Transport
of cnlcareous
fragments by reef fishes. Scicncc 133: 98-99.
BEYERS, R. J. 19163. A characteristic
metabolic
pattern in balanced microcosms.
Publ. Inst.
Mar. Sci. (Texas) 9: 19-27.
BIWECKICIX, W. S., AND T. TAI~AIIASIII.
1966.
Calcium
carbonate
precipitation
on the Bahama Banks. J. Gcophys. Rcs. 71: 1575-1602.
BUIXHMEIEU, R. W., S. V. ShJrrq AND R. A.
KINZIE III.
IN PRESS. Holocene windward
reef flat history, Eniwcl-ok Atoll.
Bull. Gcol.
Sot. Amer.
GITAVE, K. E., S. V. !hITIT, AND K. J, ROY. 1.972.
Carboaatc
production
by coral reefs. Mar.
Gcol. 12: 123-140.
CULBERSON, C., R. M. PYTKOWICZ, AND J. IX’:.
HAWLEY.
1970. Seawater
alkalinity
dctcrmination
by the pI1 method.
J. Mar. Rcs.
28: 15-21.
DOTY, M. S. 1971. Antccctlcnt
cvcnt influcncc
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Suhmitted:
27 September
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Accepted:
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1972