197
HAWAU-Y-85-004 C3
HAWAU-Y-85-004 C3
A DZSSERTATZON SUBMITTED TO THE GRADUATE DIVISION OF THEUNIVERSITY OF HAWAII IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR QF PHILOSOPHY
IN
OCEANOGRAPHY
DECEMBER 1985
By
Catherine R. Agegian
Dissertation Committee:
Keith E. Chave, ChairmanJames ArchieMaxvell Doty
Fred T. MackenzieStephen V. Smith
FAEO T. MACKENZIEDEPT. OCEANOGRAPHY
UNIV. HAWAIIHONOLULU, HI 96822
We certify that we have read this dissertation and that
in our opinion it is satisfactory in scope and quality as a
dissez=ation for the degree of Doctor of Philosophy
Oceanography.
DISSERTATION COK4fZTTZZ
Chai~ .n
ACZNOWLEDGZMZNTS
I wish to express my sincere appreciatic n to my
committee for their support, guidance, and inspiration
I was truly priviledgedthroughout my graduate program.
113
in being able to interact with this unique assemblage of
individuals.
This study was funded by the Donors of the Petroloum
Research Fund American Chemical Society', the Lerner Fund
for Marine Research, Sea Grant of Hawaii, and the
Smithsonian Institution. I am very grateful for this
support
Numerous individuals and agencies offered key
logistical support on field expeditions. The Mid Pacific
Research Laboratory and the Lawrence Livermore Laboratories
sponsored my trip to Enewetak and Bikini Atolls and provided
boat and laboratory facilities. I am especially indebted to
Lori Bell and Pat Colin for their enthusiasm and help in
working in the two most hair raising areas of theses atolls,
the algal ridge and seaward reef front. am grateful to
Martin Vitousek and Gordon Tribble for facil'ties use and
field assistance which included getting us stuck in the mud
in the middle of nowhere! at. Fanning sland. The U.S. Ccast
Guard and the U.S. Fish and Wildli e Service provided key
logist'cal support to and rom Bure Atol and :-rench ."- igate
Shoals. In addition, ping pong and pool tables provided the
greatly needed relaxation after a long hard day of diving
=ef 'geration and elec r'ci y and then hank ully, rom my
standpoint, he would fix the thing himsel . Gladys Corpuz
told me about =he sna-'' lrochus which turned out to be "he
singularly most. important component o f the microcosms,
responsible for keeping corall'ne algae healthy in
and snorkleing in the field. Both agencies generously
provided lodging, boats and food and mor~ food. Tlcyd
Venable and AMFAC Marine provided a free and unlim'ted
supply of Splash Zone Marine Epoxy which Z used to glue
half the reefs in the North Pacific Ocean back together
again.
After the fun part was over, I found myself in a clean
laboratory with about five thumbs on each hand. This
dilemma was ~wickly and expertly recti f ied by Randi
Schneider, whose guidance routinely cut my work in half.
ZoAnne Sinton generously taught me the in's and out's of
thin sectioning, despite the fact that mine always came out
kind of thick. Virginia Qreenberg provided invaluable
guidance on the analysis of calcium and magnesium with he
Atomic Absorption Spectrophotometer.
wish to express my sincere appreciation to Dr. Phil
Helfrich, director of the Hawaii Institute of Marine Biology
for supporting my experimental work at Coconut Island. My
mic ocosm experiments h nefited from the supply of 1/2" PVC
and helpful suggestions from Paul okiel and Russell to.
Wayne Nakamoto patiently taught me the magic of
captivity. Last but definitely not least, I am grateful to
Bob Young whose enthusiasm, creativity and positive thinking
helped make my ideas into phys ical realities .
Bob Cunningham and Mike Simpson helped to dispel zy
fear of CoNp~eRS.
David Robichaux was there at the bitter end when I
needed him most.
Finally, I am grateful to my family's undying support,
as I'm sure they are grateful to me for finishing with all
this--"...now will you come home?"
University of Hawaii Sea Grant CollegeProgram
Project; Ocean Dumping of Manganese NoduleProcessing Tailings: A Preliminary Assess-ment of Environmental Concerns
Project No,: ME/R � 3
ABSTRA
Coralline algae are an important world-vide component
of shallow water marine communities. They are the deepest
dwelling plant life recorded in the ocean. Therefore,
biogeochemical cycles in the ocean reservoir should include
an understanding of the factors influencing the growth and
composition of coralline algae. The effects of kinetic
growth rate! and physico-ch ical seawater temperature and
calcite saturation state! factors on the bulk magnesium
d 92 d
microcosm environments. Latitudinal variations in
g . !WILE
collections between 0 N. and 29 N. latitude. ~n situ
growth rates were obtained on the windward reef flats of
Znewetak Atoll, Bikini Atoll, Oahu, French Frigate Shoals,
and Kure Atoll. Field measurements of coralline algal
growth rate and percent cover and reef area obtained fr
charts were used to estimate carbonate production by P.
1 g 1
Hawaiian Archipelago.
Experimental results from the microcosm studies showed
influenced by growth rate but changed primarily because of
p * 1 * ~ g=
decreased at low light levels without a concomitant,
saturation states from 100% to 800% calcite s =uraticn.
settleme- of co ~lline crusts was hig.' " at calc e
saturation states between ambient �00%-500% calcite
saturation! and 772% calcite saturation.
From these experimental results, it was concluded that
and seawater temperature regimes chara-=eristic of
environmental can ions at the latitudinal e emes of reef
:owth. indeed, in situ field gr~~th measur =s indicated
.io systematic changes in growth rate betweer. . and 29
latitude as has been described for coral growth. Estimated
coralline algal production of calcium carbonate by P.
g !
the total carbonate production estimated for reefs at the
northern extremes the Hawaiian Archipelago.
importance of coralline algal and to- 1 .' '-thic ca"bonate
production is estimated and discussed n reference to the
oceanic budget of carbon.
Past and future physico-chemical changes in surface
seawater may influence the growth and composition of
coralline algae. The findings of this study suggest that
seawater may be reduced by approximately 60% if the calcite
saturation state decreases from 450% to 250% in association
with a decrease in pH from 8.2 to 7.8 and temperature
increases from 27 C to 29 C in Hawaii owing to a doubling of
atmospheric C02. The species diversity and abundance of
coralline algae in the fossil record are discussed with
respect to the past ocean environment. The appearence of
the Corallinaceae during the Pennsylvanian and Permian,
their disappearance during the Triassic and radiative
explosion at the beginning of the Cenozoic are patternes
consistent with recent reports in the literature of
oscillating trends in Phanerozoic non-skeletal carbonate
mineralogy around an "aragonite threshold".
TABLE OF CONTENTS
ACKNOWLZDGEMENTS......... ~ ............ ~ ...... ~ ...-...... ~ i:i
~ ~ ~ ~ ~ v jB S T RA CT ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ e ~ ~ ~ ~ ~ e ~ e ~ ~ ~ ~ ~A
LIST OF TABLES' ~ . ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ Xl
~ ILIST OF FIGURES ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ... ~ . ~ ~ ~ ~ ~ ~ ~ ~ eee ~ ~ ~ ~ ~ ~ ~ Xl~l
REFACE............. ~ .................. ~ ~ ~ ...... ~ ~ ~ ~ ~ .....xvP
LAT1TUDINAL VARIATIONS IN THE GROWTH AND ELEMENTAL
ENVIRONMENTAL FACTORS INFLUENCING THE GROWTH ANDMAGNESIUM CONTENT OF POROLITHON
ARD I NERZ e ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ 3 1G
IIZ. CABONATE PRODUCTION BY CORALLINE ALGAE ON HAWAZIANEFS ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ e ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ 8 3RE
IMPORTANCE OF CORALLINE ALGAE ZN THE OCEANICBUDGET OF CARBON......................... ~ ........139
CONCLUS I 0NS ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ 1 2 lV.
APPENDIX I. MAGNESIUM CONTENT FROM MICROCOSM
EXPERIMENTS e ~ ~ ~ ~ e ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ e ~ e ~ ~ ~ ~ ~ ~ e 1 2 9
APPENDIX III. SU1QGMY OF CORRECTED MAGNESIUM CONTENTSAND GROWTH RATES FROM MICROCOSM EXPERlMENTS.......164
APPENDIX IV. COMPUTER PROGRAM FOR CALCULATlNGM OLE 0 MgCO3 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ e ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ 1 6 6
BIBLIOGRAPHY........ ~ .............. ~ .................... 168
APPENDIX II. CORRECTED MAGNESIUM CONTENTS FROM MICROCOSMEXPERIMENTS........e ~ e ~ ~ ~ .-.... . - .-.. ~ ... 162
LIST OF TABLZS
PageTable
different sites in the North Pacific Ocean......ll
Correlation between temperature and 6 0
content ~ ~ ~ ~ ~ ~ ~ ~ ~ 4 ~ 4 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ' ~ ~ ~ ~ ~ ~ ~ ~ 1 ' ~ ~ ~ ~ ~ ~ ~ ~ 19
Saturometry experiments with powdered carbonate3.
minerals and seawater..........-................60
4. Functional relationships between magnesium
content and temperature for a variety of
92CalCareouS Organ1sms ~ ~ ~ .........................67
5. Percentage of reef area within reef zones.......87
6. Carbonate production by coralline algal crusts
at French Frigate Shoals, Hawaii........-.......90
and coralline algae.......... ~ ~ ~ ~ ~ ~ 93
Biogeomorphological classification of reefs in9.
the Hawaiian Archipelago.................... ~ ...97
10. Total carbonate production by corals and
coralline algae................................102
11. Shallow-water reef area in the Hawaiian
rchipelago.......................... ..,, ....113A
on Oahu, French Frigate Shoals, and Kure Atoll..91
8. Percentage of reef area covered by living corals
Carbonate production on shallow water reefs in
the Hawaiian Archipelago.......................l:4
13. Annual production of calcium carbonate on reefs
in the Hawaiian Archipelago....................l:7
l. Relative abundance of carbonate facies with
atitude..... ae ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ o3l
2. Magnesium content of calcitic organisms
at different latitudes..........-... ~ . ~ . ~ .. ~ ... ~ 5
3. Magnesium content of coralline algae at
different latitudes'� ............,..............13
with latitudee ~ ~ ~ o ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ y ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ s 1B
6. Growth rates of Porites lobata and
7. Seawater carbonate ion concentration with
t tIatitude.......................................27
light intensities..............................46
temperatures...................................49
calcite saturation states......................52
different light intensities....................54
Figure
4 ~
L1ST OF FlGURZS
C content of algal calcite and seawater
with latitude.....................
6 0 content of algal calcite
d'
Page
~ ..16
fferent temperatures............., ..........56
different calcite saturation states. ~ ...... ~ ...59
14. Diel variations in the calcite saturation
state of seawater over a reef flat
in Zaneohe Bay.................................63
15. Contour plot of magnesium content as a functio~
of te rature and calcite saturation state....77
16. Oscillations in non-skeletal carbonate
mineralogy, sea leveL and the abundance of
calcareous red algae throughout the
P hanerozoj.c....................................81
rchipelago.................. ~ . ~ .,............104A
19. Percentage of total carbonate pro action on
reefs in the Hawaiia~ Archipelago
attributable to coralline algae ~ ~ ~ ~ ~ 1 06
Xiv
17. Nap of the Hawaiian Archipelago............... ~ 86
18. Total carbonate production by corals and
coralline algae on reefs in the Hawaiian
PRZFACE
The dissertation topic presented herein has evolved
through a series of discoveries and rediscoveries. The
significance of these discoveries was not always immediately
obvious.
discovered for myself that there are mass've
carbonate formations called coral reefs, that are composed
of the fossil remains of calcareous organisms. I discovered
that the term, "coral reef", was a misnomer, and
subsequently I have used the term, "biotic reef". I learned
that the predominant mineralogical forms on biotic reefs
such as aragonite and magnesian calcite calcite with a high
magnesium content! were metastable at Earth's surface
temperature and pressure and over a geologic time scale
these phases should eventually be converted to calcite or
dolomite. X discovered the fossil record, the pez'served
autobiography of a reef or individual calcareous organism,
and subsequently came to appreciate geologic time.
These discoveries led to my curiosity about =he
interactions between calcareous organisms and seawater.
This initially diffuse intezest has resulted in my
dissertation topic, "The biogeochemical ecology of he
interests encompassed by this title are discussed below. The
"biogeochemical" component of this title, like stereoscopic
provided a three-dimensional overlay of hevision,
separate fields of study, biology, geology and chemist.
relating the interactions between calcareous organisms,
seawater, and the geologic record.
The use of coralline algae in this study, the
from the realization that biotic reefs were composed of many
types of calcareous organisms, not just corals. I became
aware of the ubiquity of coralline algae in these systems
and wondered about the reas :s for their apparent success.
Once I started to see pink, coralline algae appeared out of
nowhere-- on the shallowest intertidal basalt or carbonate
substratum, on the undersides of rocks buried in the sand,
at the deepest depths recorded for plant life in the ocean.
Of course I wasn't the first one to note their abundance.
Pollock l928! quantified the predominance of coralline
aLgae on Hawaiian r =s. Si 'equently, n amer ous
investigators {e.g Littler, 1985; Sog~ iartc. 1972; Adey and
Vassar, l975! studied the ecologic significance of coralline
algae on biotic reefs. Coralline algal abundance has been
identified on fossil reefs. The first deep reef coring, in
the central Paciic at Funafuti, demonstrated that crustose
coralline algae can be a dominant framebuilding organisms on
tropical reefs Finckh, 1904! . A similar picture was
obtained for both the Recent and Tertiary rocks on the
world's most northern atolls, Midway and Kure in the
Hawaiian Archipelago Gross et al., 1969 Ladd et al.,
3.967! .
In addition to their abundance, coralline algae were
easy to collect and did not produce copious amounts of
slime upon the slightest perturbation, a response
characteristic of hermatypic corals. Furthermore, 1 had
absolutely no qualms about smashing them into little piece
which I was sure I would have to do sometime during the
course of my research. The branched coralline alga
y' ' ' d ' ' y
fulfilled all the above requirements, in addition to a more
practical requirement, I could give it a positive taxonomic
identification in the field.
The "ecology" component of this title provided the
opportunity to ask questions of particular significance to
me: "How does the ocean influence the life of the
organism?", "How does this calcareous organism influence the
biogeochemistry of the ocean reservoir?", and by addressing
these questions, "How will anthropogenic or man-induced
changes in the global environment perturb the ocean system
which I had defined?".
The sum of these initial discoveries led to he
realization that coralline algae were an important component
of shallow and deep water marine communtities world-wide.
Therefore, biogeochemical cycles in the ocean reservoir must
XVii
include an understanding of the factors influencing the
growt ind composition of coralline algae.
Zn Chapter I, the results of measurements of natural
variations in growth rate, magnesium content, and stable
P S
latitude are presented. The growth rate and elemental
over this latitudinal range arecomposition of P.
compared with regional and local variations in temperature
and seawater saturation state. Hulk magnesium contents of
p h d
temperate to subarctic species of coralline algae,
~laciale ahd with values reported by Chave
f 1'
biogeochemical ecology of the organism. The effects of
solar radiation, temperature and calcite saturation state an
were examined experimentally in controlled microcosm
Experimental results presented in thisenvironments.
chapter are used to evaluate the percentage of natural
�954! for several species of coralline algae over a similar
latitudinal range.
In Chapter EI, a controversy is addressed: Is the
magnesi ~ content of calcitic organisms influenced by
kinetic factors growth rate! or physico-chemico factors
seawater temperature and calcite saturation state!. In
addressing this controversy I hoped to learn what role the
variation in bulk magnesium content that can be explained
by these environmental factors.
In Chapter III, the importance of carbonate product'on
by coralline algae is estimated at the northern extremes of
reef growth, on Hawaiian reefs between 19 and 29 N.
latitude. In situ growth rate measurements reported in
Chapter I are used in conjunction with field estimates of
and coralline algal cruststhe percent cover of P,
within specific zones on reefs throughout the Hawaiian
Archipelago to estimate carbonate production on individual
reefs. The importance of carbonate production by coralline
algae throughout the Hawaiian Archipelago is estimated.
Coralline algal production is compared with coral production
estimated from Grigg {1982! made on these same reefs.
ln Chapter IV, shallow water carbonate production by
coralline algae and corals is compared to estimated
carbonate production on deep water banks in the tropics and
subtropics as well as temperate regions to evaluate the
importance of benthic carbonate production in the global
budget of carbon.
Chapter V summarizes the major findings of this study.
The biogeochemical ecology of coralline algae is discussed
with respect to past, present. and future ocean environments.
I. LATITUDINAL VARIATIONS IN THE GROWTH AND ELEMENTAL
COMPOSITION OF POROLITHON GARDINERI
INTRODUCTION
The relative abundance of calcareous organisms in
sedimentary carbonate facies varies with latitude Schlanger
Corall'neand Konishi, 1975; Lees and Buller, 1972!.
red algae, calcareous green algae, foraminifera and
hermatypic corals are the dominant producers of calcium
carbonate in the warm, shallow seas of most tropical
oceans. Hermatypic corals and calcareous green algae become
rare at high latitudes and are replaced by bryozoan-rich
facies Schlanger and Konishi, 1975; foramol association,
Lees and Buller, 1972!. The coralline red algae,
unlike hermatypic corals, calcareous green algae or
bryozoans, contribute significantly to sediments at all
latitudes Figure l!.
The overall mineralogical composition of biogenic
carbonate facies also varies with latitude. Relatively
soluble carbonate minerals, such as aragonite and calcite
with a high magnesium content, are abundant in tropical
seawater highly supersaturated with respect to calcite
minerals Milliman, 1974; Lowenstam, 1964; 1954!. At high
latitudes, the magnesium content of coralline algae and
other calcitic organisms is low Figure 2!; the magnesium
FIGURE 1. Relative ahundance of calcareous organisms incarbonate facies adapted from Schlanger and Konishi, 1975!
LN>Qva8~ vOww03 38~8
33NvGNAGV GAIT.vl38
. l
FZGURE 2. Latitudinal distribution of magnesium content inbiogenic magnesian calcites. figure from Mackenzie et al.
1983; data from Crave,1954!
25
10
10
0
g! 20
o~
0]$
20 30 40 50 60 70LATITVDE 'N
content increases with decreasing latitude. Chave �954!
concluded that the magnesium content of calcitic organisms
was influenced primarily by physico-chemical factors because
he found positive linear relationships between magnesium
content and temperature in many groups of organisms.
Noberly �968! proposed, however, that growth rate was the
major factor influencing the magnesium content of coralline
algae, and that temperature or other environmental factors!
acted indirectly in influencing growth.
In general, carbonate production is higher on coral
reefs than on rocky shores in temperate regions Smith,
1972! . The geographic distribution of tropical
calcareous organisms is generally believed to be influenced
by regional variations in environmental factors such as
solar radiation and temperature Goreau, 1963; Wells, 1957!,
Low temperature and solar radiation regimes characteristic
of high latitudes may inhibit growth Jokiel and Coles,
1977! and reproduction Grigg et al., 1981! of hermatypic
corals. Grigg �982! measured a linear decrease in the
growth of the hermatypic coral Porites lobata between 19
N. and 29 N. latitude; he hypothesized that reduced light
and temperature regimes at the northern extremes of reef
growth in the Hawaiian Archipelago limited the growth of
this species.
Few investigators have measured the growth of tropical
cor' line algae in the field. Adey and Vassar �975!
determined marginal extension rates of 1 to 2.3 mm/month
for shallow water, tropical, crustose coralline algae.
8 mm/yr Steneck and Adey, 1976!. No systematic study,
however, of the growth of a single species of coralline
algae with latitude has been undertaken.
Based on the above considerations, it was hypothesized
that: l} the growth and geographic extent of stri,c ly
tropical/subtropical genera of coralline algae are
influenced by environmental factors in the same manner as
that described for hermatypic corals, and 2! magnesium
content decreases with increasing latitude in conjunction
with regional variations in temperature.
P
measured in situ, on reefs between 10o and 29 N. latitude.
The magnesium content and stable carbon and oxygen isotopic
composition of Porolithon skeletons were determined for use
as potential indicators of environmental growth conditions
over the total geographic range between 0 and 29 N.
latitude inhabited by this species in the North Pacific
Ocean. Field measurements of growth and elemental
composition are discussed with respect to the importance of
regional versus
conditions.
local vaz'iations in environmental
METHODS
Growth Studies:
The growth of the branched coralline alga Porolithcn
Enewetak �1 N. latitude! and Bikini {11 N. latitude!
atolls, Marshall Islands and Oahu �1 N. latitude!, French
Frigate Shoals FFS, 23.7o N. latitude!, and Kure Atoll
�8.4 N. latitude!, Hawaiian Archipelago. At each
and stained with Alizarin Red S at a conc ntration of 0.25 g
stain liter . A detailed description of the staining
procedure is given in Chapter II. During the staining
period � hours! each plant was attached to a 1 l/2"
diameter x 1" thick PVC ring with Splash Zone Marine Epoxy
Z-spar or Kopelands!. After staining, the plants were
returned to the field and attached directly to the reef with
stainless steel hose clamps. The hose clamps were threaded
through two opposing slits previou= .y sawed at the base of
PVC ring. The hose clamp was then tightened around a solid
portion of the substratum. The stained plants were left on
the reef flats for variable lengths of time Table 1!,
depending on the investigator's ability to return to a
specific site, some of which are quite remote.
Although care was taken to place the plants at the same
depth at all sites, small variations in depth were
inevitable. For instance, in the Marshall Zslands Enewetak
ridge. This ridge is exposed at low tide. Alizarin stained
plants were secured in these areas and may have been exposed
during low tides. Certain portions of the reef flat at
French Frigate Shoals may be exposed during low tides,
however, much of the reef flat is subtidal. In situ growth
rates were measured from plants which were secured on the
deeper portions of the reef flat and it is unlikely that
they were exposed at low tide. In contrast, stained P.
d
never exposed at water depths less than 1.5 m.
Growth rates were determined from two sectioned t'ps
per plant as described in Chapter II. Sample size
n ~ 4 of plants! was dependent on the number of plants that
remained at each site over the period of the investigation.
Magnesium and Calcium Analysis:
Bulk magnesium content was determined by atomic
absorption spectroscopy according to the methods outlined in
Chapter II. Small scale variations in magnesium content
within 20 micron diameter spots on the skeleton! were
measured with an electron microprobe. Standard operat' ng
conditions for the electron microprobe were as follows: 15
kv accelerating potential, 20 second counts, and 0.15 A
filament current.
Stable isotopi. =omposition:
Isotopic analyses were performed with a mass
spectrometer at the University of North Carolina. Carbonate
C and o 0 results are reported relative tc the PDB
isotopic standard.
RESULTS
~ 1 f
Oahu and only slightly lower on French Frigate Shoals and
Kure Atoll Table 1!. Growth rates measured on Bikini and
Enewetak were similar to each other and on the average 40%
lower than the average growth rate measured in the Hawaiian
Archipelago. Overall, the growth rates of Porolithon
measured on different reef flats in the Hawaiian Archipelago
are remarkably similar considering the variation in growth
periods and total number of days that the plants remained in
the field.
The bulk magnesium content measured by atomic
absorption spectrometry circles, Figure 3! ranged between
14.5 and 20.5 mole % KgC03. The magnesium content of
N. latitude. The magnesium content determined by electron
microprobe was, in general, higher than the bulk values
determined by atomic absorption spectroscopy Figure 3!.
The total range in magnesium contents measured by electron
microprobe was about 14 mole % MgC03, about 8 mole % NgC03
10
ca N
CO h CO
Ol
O0
i
C4 0
co AI I
Q
Q 0 H N VJ
h
U
O Ih h
P4 IllCh
0 0
00 N
0
~ W QeQ
W U0 0
gE
0H 3
H
Q
ru0!
CV"lo a
IP A W8
& G4
11
QOa
44HH
4lC OM
'UU 4
tO O
R NOSXl4V 84W444l ai
5NN Q
ra44 Cl~
C 4l'6AM 0
Q.H 4
8
Ctd C
0 0 0 0 0 0 0P4 & Fl h4
0! W W 0D Pl pl O N Fl
0 0 0 0 0 0 0
Cl Fl 0 p!~ W Lh
~ ~H H H + A 0 57
FIGURE 3. Magnesium content of coralline algae withlatitude. Circles: Atomic absorption spectroscopy,
~ r, a: ' wmicroprohe analysis, Lithothamnium Slaciale, Squares: X-raydiffraction analysis, coralline algae adapted
from Chave 1954!
O o C!
0 4
~oo~w x s>ow3.3
higher than the i k measurements. The highest magnesium
contents determined by atomic absorption spectroscopy or
electron microprobe were between 2lo and 29 N. latitude.
The stable carbon isotopic composition of Porolithon
was fairly constant at all sites except Christmas Island
� N. lat.!, Bikini �1 N. lat.! and Johnston �5 N. lat.!
Atolls where the skeletons of this alga were isotopically
heavier Figure 4!. The stable carbon isotc pic composit on
of seawater from the NORPAX expedition, LEGS 7, 11, and 15
Tilbrook, 1982!, followed a similar trend with latitude.
Porolithon skeletons were enriched in 0 0 relative to
0 with decreasing latitude Figure 5!. The maximum and
minimum average temperatures recorded at each site Table 2!
were averaged and used to derive a geometric mean regression
between P
skeletons. The ,j 0 value for Bikini was not incorporated
in this equation because of the uncertainty of the
environmental temperature of the semi-exposed habitat from
which this specimen was collected. The resulting equation
describes the average median temperature as a function of
average 6 0 composition:
T C!= 20.3 � 1 41 o 0:
r = 0.90, n=7.
FIGURE 4. ~ C isotopic composition of
CO2 of surface seawater samples during NQRPAX legs ll and15 crosses; adapted from Tilbrook, 1982!
15
C!
O
Z
C!
C!
C!
I
16
00
C!
aad "~}~'z�g
{sad'-i} r�g
00
C!
FIGURE 5. 6 0 isotopic composition of PorolithonILK
17
CVl 1
CVI
18
CQ
I
43
I
GGd '%! Q,Q
00
I
TABLE 2. Stable ' O isotopic composition of ~c ~theo~a d~i e~r and associated average maximum and minimumtemperatures for each site. The average median temperaturewas determined as the sum of maximum and minmium values
divided hy two
i 18OLOCAT ZON
S. D.
28 ~ 7JARVZS 2 6. 0 -4 ~ 31-4. 43-4 ' 61
27.4
-4 ~ 45 0 ~ 15
25.828.0XKAS 23. 5 4. 15-4. 20-4.22
-4 19 0 04
FAHNZNG 24.8 26.728 ' 5 -4.53-4.60-4 ' 75
4.63 0.11
JOHNSTON 24.5 28 ~ 5 26 ~ 5
-4.50 0.16
-3.27-3.45
25. 0OAHU 2 1 ~ 5 27 ' 5
3,36 0.13
27.5 25 ' 0
3.49 0.11
KLRZ ' 8. 5 28. 5 23 ~ 5
-2.25 0 F 08
BZEZÃZ
-3.57 0.15
19
TEMPERATURE
AVG.MZN. AVG.KAX. AVG.MEDZAN
4.32-4.55-4.63
-3 ' 393.47
-3 ' 61
-2.172.24
-2.33
-3.41-3 ' 60-3.71
1 ISCUSSION
The growth of Porolithon did not vary systematically
with latitude. Over the entire range of latitudes examined,
growth rate was highest on Oahu �1 N. latitude!. Growth
rate was lowest at low latitude sites in the Marshall
Islands Bikini and Enewetak!. An intermediate growth rate
was measured at high latitude sites �3 and 28.4 N.
latitude! for this species. These resu3.ts suggest tha
' ~
variations in environmental factors, such as temperature and
solar radiation, and/or 2! local variations in environmental
factors influence growth rate, and hence obscure the
effects of regional variations.
Variations in the growth rate of Porolithon between the
Marshall Islands and Hawaiian Archipelago may result from
3.ocal, microhabitat differences. Enewetak and Bikini are
mature atolls with well established windward. ridges. In
contrast to sites in the Hawaiian Archipelago, Porolithon
grows intertidally in these locations and is probably
subject to periodic exposures to the atmosphere during
periods of low tides. This view is further supported by
visual observations of the external morphology of the
plants. At Bikini and Enewetak, individual p3.ants are
massive and have thick branches. Smith and Harrison �978!
noted that calcification rates on coralline algal pavements
out of the immediate turbulence of the algal ridge were
20
greatly reduced, very possibly a result of this same
ardineriphenonmenon. In general, the branches of P.
observed growing on subtidal reef flats in the Hawaiian
Archipelago were long and thin. Steneck and Adey �976!
followed the change in branch morphology of the coralline
from deep water sites to intertidal sites was stunted
resulting in increased horizontal carbonate accretion around
individual branch tips.
Relatively small variations in the growth rate of
Porolithon were observed between all sites within the
Hawaiian Archipelago. Growth rate decreased slightly between
21 N. and 28.4o N. latitude. For comparison, the grovth
rate of the hermatypic coral ~Po 'tes ~loh t decreased
dramatically between 19s5 and 28s4 N. latitude Grigg,
1982! in the Havaiian Archipelago. The latitudinal trends
g ' 1 1'
summarized in Figure 6. Grigg �982! suggested that reduced
light and temperature regimes vere the major factors
influencing the growth of Porites at high latitudes.
Reductions in incident solar radiation had relatively small
effect on the growth of Porites grown in controlled
21
microcosm environments Houck et al., 1977!. The growth of
~por tes lo'hate, however, was reduced hy approximately 504 at
22.5 C in comparison to its grovth at 27 C in controlled
F1GURE 6. Overall trend iz the grovth of Porolithonh
Kure. Average trend in grovth of Porites lobata pithlatitude established by the equation: GROWTH RATE mm y !
33.5 - 1.08 LATITUDE N.! from Grigg �982!
22
!vironmehtmlcrocc .ouck et al., 1977!. The growth of
Parali: , in contra .d microcosm experiments did not vary
under light or temperature regimes characteristic of
latitudes at the northern extremes of reef growth Chapter
II!. Growth rate was fairly constant between 23 and 28 C.
Zn view of the experimental data reported in Chapter II, a
decrease in in situ -awth rate of Parolithc would nat be
24
effected vithi th .verage latit iinal te ature range
in the Hawaiian Archipelago.
Latitudinal variations in stable carbon isotopic
composition of Poralithan skeletal material were consistent
with the overall trends in stable carbon isotopic
composition measured in open ocean surface seawater by the
NORPAX expedition, legs 7, 11, and 15 Tilbrook, 1982!.
This observation would indicate that Parolithon skeletons
are precipitated fram open-ocean seawater removed fram any
local variations in the physico-chemical properties of
seawater.
The trend in skeletal oxygen isotopic composition is
consistent with this notion and suggests that Poralithan is
at least recording regional variations in temperature. The
relationship derived in this study, however, is different
than both empirically derived relationships and equilibrium
equatic .eported in the literature. Weil et al., l981!
derived the empirical relationships:
T C! = 3.76 - 4.29 6 Qc 5 Ow!
T C! 3.58 - 4.61 '~ c ~ w!
respectively. The slopes obtained by Weil et al. �981!,
Weber and Woodhead l972!, and Dunbar et al. �980! were not
dramatically different from each other or from the
equilibrium equation, although cozals do show a
taxonomically consistent offset i.e., intercept values!
from the equilibrium equation. The coralline algal
temperatuze coefficient is only approximately one third that
of the cozals; therefore, the "thermometer" is both less
sensitive and offset. isotopic fzactionation in magnesian
calcites may be influenced, however, by magnesium content
Tarutani, 1969!. Zn any event, future studies should be
designed to define the coralline algal "thermometer" with
0 values from plants grown under controlled temperature
conditions.
Zn contrast, the magnesium content of Porolithon does
not appear to be recording a temperature signal. The bulk
did not decrease between the equator and 28.4 N. latitude
despite a regional decrease in temperature.
Carbonate ion concentration Figure 7! exhibits a
similar trend over the latitudinal range investigated.
Carbonate ion concentration, a measure of calcite saturation
state, is highest within subtropical latitudes and lowest at
high latitudes oz within the vicinity of the the equatozial
FIGURE 7. Carbonate ion concentration of seawater as afunction of latitude. adapted from Broecker et al., 1979!
Q < ev oo
0
6I ~~IO" ~ Olx! -<F03
upwel g zone. Recer;vestigatic Schoon. ar, 1981;
Walte-, 1983! sugg. that surf seawater is not
supersaturated with respect to calcite with a high magnesium
content. Expezimental evidence presented in Chapter II
suggests that the calcite saturation state of seawater is a
primary factor influencing growth and magesnium content in
Porolithon therefore, magnesium content may be influenced by
regional variations in saturation state. A correlatior
between carbonate ion concentration and magnesium content is
suggested by the generally high magnesium values determined.
te have been measured in individual shoal-saturation
water environments Smith, 1981; Kinsey, 1979; Smith and
latitudinal variations in saturation state may influence
the magnesium contempt of Porolithon. Figure 3 also shows
the x-ray diffraction values determine by Chave �954! for
sevezal genera of coralline algae' The highest magnesium
contents he reported occurred at subtropical latitudes off
Flozida. Considering all data sho. n in 'igure 3, the
highest magnesium values were consistently sured in the
subtropical region of the North Pacific Ocean, between 21o
and 33o N. latitude.
The range in magnesium contents measured in Porolithon
at a particular site also suggest that local variations in
environmental conditions may influence the natural variation
in skeleta' pnesium content. Local vaziations in seawater
Pesret, 1974; Schmalz and Swanson, 1969; Broecker and
Takahashi, 1966!. A measure of the importance of local
variations as opposed to regional variations in physico-
chemical factors on individual reefs could be determined
only by an intensive field monitoring program which was not
conducted as part of this study. Zt can only be concluded,
therefore, that the field measurements of elemental
composition suggest that regional and local variations in
physico-chemical factors may influence the growth and
!n conclusion, the bulk magnesium content of Porolithon
is not a particulary good indicator of latitudinal changes
in temperature, possibly owing to the combined effects of'
local and regional variations in calcite saturation state.
Stable oxygen isotopic composition of Porolithon, however,
is correlated with regional seawater temperatures.
Controlled microcosm experiments must be conducted to
identify the effects of calcite saturation state and
temperature on the growth and magnesium content of
Porolithon Chapter ZI!. Field measurements of growth rate
indicate that coralline algal growth is high at latitudes in
which coral growth becomes attenuated. This suggests that
P Y 1
crusts may be significant on reefs throughout the Hawaiian
Archipelago Chapter ZZI!; a conclusion substantiated by the
observed predominance of coralline algal skeletal material
29
in sha11ow reef sediments in the Northwestern Hawaiian
Islands Gross et al., 1969!.
30
II. ENVIRONMENTAL FACTORS INFLUENCING THE GROWTH AND
INTRODUCTION
The magnesium content of coralline algae and other
calcitic organisms in general decreases with increasing
latitude {Figure 2!. This seemingly simple relationship has
generated numerous questions concerning the precipitation of
biogenic magnesian calcites from surface seawater since the
classic work of Clarke and Wheeler �917!. Although
latitudinal variations in magnesium content are well
established see Mackenzie et a1.,1983, for review!,
investigators have not agreed upon what factors influence
the magnesium content of calcitic organisms. Disagreements
have been couched in two camps: 1! The magnesium content of
calcitic organisms is the result of physico-chemical
factors, e.g. temperature, and 2! The magnesium content of
calcitic organisms is influenced by biological kinetic
factors e.g. growth rate. Growth rate is, in turn,
influenced by biological, physical and chemical factors.
Chave l954! showed a correLation between the
magnesium content of calcitic organisms with temperature.
He inferred that the magnesium content of calcitic
skeletons was influenced by physico-chemical factors because
positive linear relationships between magnesium content and
temperature were described in many groups of organisms.
31
Chave and Wheeler �965! correlated seasonal variations in
magnesium content in the skeleton of the coralline alga,
Cl th om gRMlltgR, 1th t . *h
latitudinal variations in magnesium content may be
influenced physico-chemically by temperature.
Zntraspecific between different skeletal parts of one
organism or between individuals of the same species!
variability in the magnesium content of calcareous organisms
suggested that, a strictly physical-chemical model describing
a direct relationship between skeletal magnesium content and
seawater temperature was insufficient Moberly,1968; Weber,
1973!. Extensive analyses of echinoid and asteroid skeletal
parts showed that intraspecific variability was a function
of particular skeletal components Chave, 1954' Weber,
1973!. The teeth and spines of five tropical sea urchin
species had a relatively low magnesium content in comparison
to the tests Weber, 1973!. Zn other cases, spines had a
higher magnesium content Chave, 1954! than tests.
Noberly �968! challenged the physico-chemical
hypothesis based on electron microprobe studies by proposing
that growth rate was the major factor influencing the
magnesium content of coralline algae. He concluded that a
high magnesium content would result under high growth rates
because coralline algae are less able to discriminate
against magnesium which is five times more abundant than
calcium on a molar basis in seawater. Moberly correlated
32
variations in magnesium content with variations in skeletal
growth patterns which he considered a measure of the rate at
which calcite was precipitated. Kolesar l978; 1973! also
concluded that growth rate was probably the major factor
controlling the magnesium content of algal calcite; however,
in contrast to Moberly's conclusions, low magnesium content
was correlated with periods of rapid growth. Kolesar �973!
correlated growth rates of coralline. algae reported in the
literature with his atomic absorption spectrophotometric
analyses of magnesium content of algal skeletons of the same
genera.
The ability to distinguish between kinetic and physico-
chemical factors influencing magnesium content in calcareous
organisms is complicated by the fact that many
environmental factors influence growth. The CaCO>
production rate of calcareous organisms may be slightly
lower in temperate regions than in the tropics Smith,
1972!. Regional variations in environmental conditions might
influence the growth of calcareous organisms and hence,
their magnesium content. Grigg �982! zeported a simple
linear decrease in the growth rate of the hermatypic coral
~Po ~es lobata with increasing latitude. Grigg and Dollar
�980! suggested that light and temperature probably limited
the growth of carals at high latitudes. Several
investigators have shown that coralline algal growth is
influenced by the same environmental factors as corals.
33
Maksaki et al. �981! showed that the growth rate of
temperate water species of coralline algae decreased with
decreasing temperature, whereas light intensity had little
effect on the growth of these species. Soegiarto �972!
measured, decreases in growth rate of several species of
tropical coralline algae under reduced light conditions.
Therefore, latitudinal variations in magnesium content of
calcitic organisms may be i.nfluenced kinetically by changes
in growth rate in response to a number of environmental
conditions.
The carbonate chemistry of seawater has usually not
been considered to be an important regional physico-chemical
or kinetic factor influencing the biogenic precipitation of
aragonite or calcite because surface seawater is
supersaturated with respect to these minerals. The study by
Smith and Pesret �974! of the Fanning Atoll lagoon is an
exception to this generality. Recent investigations
Schoonmaker, 1981; Walter, 1983!, however, suggest that
surface seawater is not supersaturated with respect to
calcite with a high magnesium content. The carbonate
saturation state of seawater is defined with respect to a
particular carbonate mineral as the product of the
concentrations of Ca and C03 ions in seawater divided by
the apparent solubility product for the mineral Cloud,
1965!. The carbonate saturation state of surface seawater
is influenced primarily by the C03 concentration of
seawater because Ca + ion concentration varies by less than
10% in open ocean water. The CO3 ion concentration varies
with latitude Figure 7; Broecker, et al.,1979!. At high
latitudes, the solubility of CO2 increases with decreasing
temperature; hence the CO3 concentration decreases.
Cold, CO2-rich upwelling equatorial water produces a similar
effect near the equator. In warm, subtropical and tropical
waters removed from the equatorial influence, the CO3
content is at a maximum. In addition, biologically mediated
processes also influence the carbonate saturation state of
seawater. These processes, such as photosynthesis,
respiration, calcification, and carbonate dissolution may be
important on a local scale Smith and Pesret, 1974; Schmalz
and Swanson, 1969; Broecker and Takahashi, 1966!.
Carbonate ion concentration may influence the growth
rate of coralline algae Borowitzka, 1981: Smith and. Roth,
l979! and hence their magnesium content. Several
investigators have attempted to elucidate the role of the
C02 system in coralline algal growth Borowitzka, 1981;
Smith and Roth, 1979; Notoya, 1976!. To date, the results of
these studies have been inconclusive. Using short-term
hours! C incubations, Borowitzka �981! studied the
effect of pH on calcification rate in an articulated
coralline alga at two pH treatments, 7.2 and 8.3. Rates
measured at unnaturally high pH values up to 10! were
suspect because calcification was markedly higher in dead
control plants. Based on the above it seems probable that,
local and regional variations in the carbonate saturation
state of seawater may influence the precipitation and/or
composition of biogenic magnesian calcites.
The resulting picture of the factors controlling the
magnesium content of calcitic organisms is confusing, at
best. Weber �973! concluded, "There is, unfortunately, no
direct and unequivocal- proof that growth rate is truly the
fundamental cause of variations in the chemical composition
of biogenically formed carbonates." Mackenzie et al.,
l983! emphasized that, "There is a strong need to assess
quantitatively the crystal chemistry of naturally occurring
magnesian calcites, in conjunction with physical and
chemical environmental factors and vital effects".
The prese~t chapter examines, experimentally, the
effects of kinetic growth rate! and physico-chemcial
temperature and calcite saturation state! factors
incluencing the growth and composition of the coralline alga
EXDlljig ~ . th
discussed with respect to the role of skeletal magnesium in
11m 1 1 1 ~~ ~
METHODS
Experimental Microcosm Procedure:
All experiments were conducted at the Hawaii Institute
of Marine Biology HZMB!, at Coconut island, Hawaii. The
d lit, ZZJJJgl
l dd ddt tdd l,
because it grows abundantly on the vindward reef flat of
Kaneohe Bay, a 10 minute boat ride from the laboratory
ly.~ l ~
tropica3. reef crest and reef flat environments throughout
the tropical and subtropical North Pacific, but may occur at
greater �9 m! depths Adey et al,, 1982!.
The microcosm system consisted of twelve identical,
plexiglas cubica3. tanks approximate volume 27 liters!
exposed to natural sunlight and. continuously floving natural
seavater. All seawater supply lines were made of PVC.
seawater flow rates in al3. tanks were identical and
adjusted by PVC ball valves. Seawater supplied to the tanks
was never exposed to metal of any kind. High seawater flov
rates �.0 liters min ! minimized diurnal temperature
fluctuations and changes in water chemistry aving to plant
activity. Grazing fish and snails vere included in each
tank to control the biomass of rapidly growing filamentous
algae. Homogeneous seawater composition and temperature
within each tank was maintained by mixing using a magnetic
stir motor attached to the bottom of the tank and a stir bar
in the tank.
Growth rates were determined by staining individual
sell � " 'dd ' '" t d*
for four hours. Ten algal heads vere used for each
37
experiment. Each head was separated into as many clusters
of branches as there were individual treatments. Prior to
staining, each cluster was mounted. on l/2-inch PVC pipe
rings with underwater marine epoxy. Rapid seawater flow
rates were maintained until the epoxy hardened to minimize
the concentration of chemical by-products produced during
the curing process. After the staining period, the rings
with algal clusters attached were secured on 1/2-inch PVC
couplings that had been previously mounted vithin each tank.
Therefore, the genetic composition between tanks was
identical. The effect of underwater marine epoxy on growth
rate was assumed to be minimal because contact with the
plant was only at the base, some distance from the growing
tips. Adey �978! used this epoxy in field studies of
coralline algal growth rates with no apparent detrimental
ef fects. Andrake and Johansen �980! determined that the
growth rate of an articulated species of coralline algae was
not influenced by staining vith Alizarin Red $.
Experiments were typically run for 20 to 27 days, after
vhich tips from the branches were sectioned and the distance
between the stain mark and the apex of the branch tip was
measured using an occular micrometer in a dissecting
microscope. This distance divided by the number of days
over which the plant grew represents the mean vertical
extension rate. Rates vere determined for 10 plants from
three tips/plant Experiments I and ZI!, and four tips/plant
38
Experiments IIZ, EV, V!, The largest standard error about
any mean growth rate for any temperature treatment was 0.04
/ th .* I g
the tanks representing ambient growth conditions �.5
mm/month! was slightly higher than field growth rates
determined at sites near the laboratory �.2 mm/month;
Chapter I!.
Different seawater saturation states between 100-860
calcite saturation were administered to each tank by
metering in different amounts of HCl and NaOH with a
peristaltic pump. Carbonate saturation state is given with
respect to calcite using the ksp for calcite from Plath et
al. �.979!. Percent calcite saturation was calculated from
measured values of pH and alkalinity at ambient temperature
and 35 /oo salinity. Calcite saturation state variation
during individual experiments in all tanks was about 6%
Temperature extremes ranging from 19.5 to 30 C were
produced by allowing seawater to flow through a series of
glass tubes coiled inside cold and hot temperature baths.
Intermediate temperature regimes were furnished by mixing
water of extreme temperature with ambient seawater.
Temperature variation within individual tanks was about
+0 5 CD
Light treatments were administered by shading
individual tanks with neutral density filters. Light
treatments within each chamber were calibrated in natural
39
sunlight with two Licor light meters, used simultaneously.
Photon fluence was measured vith a spherical light sensor
inside the seawater-filled chamber and compazed to a light
reading made simultaneously with a flat sensor measuring
photon flux located outside the tank. A spherical light
sensor that measures photon fluence! was used rather than
a flat sensor that measures photon flux! to provide a
better estimate of the total light envizonment inside each
tank. Each light treatment vas calibrated in this manner to
account for rapid changes in natural sunlight because of
passing clouds. Solar radiation is reported as 4 surface
illumination. The highest light treatment no neutral
density filter! was comparable to light levels measured on
the shallow �.5 m! reef flat immediately adjacent to the
chambers and perhaps higher than in the breaking waves where
the alga grows.
Direct seawater satuzometry experiments after Weyl,
Jllllsl ~ p d 1th
about 18 mole 4 MgCO> and calcite powder. Seawater at
different calcite saturation states! vas taken from the
microcosm experiments and. placed in a beaker with a magnetic
stir bar. The pH of seawater samples at 25 C was measured
before and after the addition of an abundance of powdered
carbonate mineral.
The change in calcite saturation state vas calculated
over a 24-hour period from a fixed site on a windward. reef
40
flat near Kappa Island in Kaneohe Bay depth 1.5 meters!.
Saturation state was calculated from pH, alkalinity,
salinity and temperature measurements taken on an hourly
basis.
Sample Preparation for Atomic Absorption Spectroscopy:
Algal tips sectioned f or growth rate determinations
vere analysed by atomic absorption spectroscopy for
magnesium and calcium. Coralline algal skeletal material
was broken from the outer tip of the algal beyond not
including! the Alizarin stain mark.
Approximately one milligram of skeletal material from
each tip was weighed out and placed in disposable, conical,
15 ml centrifuge tubes containing 304 H202 hydrogen
peroxide!, buffered with NaOH sodium hydroxide! to a pH of
5.5. Centrifuge tubes with the algal samples were placed in
a test tube rack in an ultrasonic bath and sonicated from
one half hour. After one hour, the tubes were rinsed with
doubly-distilled water and dried at 60 C overnight.
Samples vere dissolved in 200 pl concentrated "intra-
analysed" HCl and diluted to 10 ml with doubly-distilled
water. One ml aliquots of these samples were transferred to
new centrifuge tubes with potassium chloride KCl! solution
{54 of the total volume!, lanthanum chloride solution {15%
of total volume! and doubly-distilled water diluted to
total volume of 10 ml! to provide a constant matrix effect.
41
Potassium chloride solution vas made from 38.10 grams of KCl
dissolved in doubly-distilled water and diluted to one liter
in a volumetric flask. Lanthanum chloride solution was made
one day in advance of analysis by dissolving 58.65 grams
La203 in a one-liter volumetric flask with a small amount ofdoubly-distilled water. Gradually and carefully! 250 ml of
concentrated HCl was added. in 25 ml increments, and diluted
to almost one liter with doubly-distilled water. The
dilution was completed the following day to account for the
volumetric effects of thermal expansion. Blank solutions
were prepared at the same time with KCl, La202, HCl and
doubly-distilled water. Background magnesium and calcium
concentrations determined from the blanks were subtracted
from the sample concentrations. Blank solutions contained
less than 0.001 ppm Mg and 0.01 ppm Ca.
Analytical standards were prepared from "Baker instra-
analysed" 1000 ppm atomic absorption standard solutions.
One ml of 1000 ppm Mg stock solution and 10 ml of 1000 ppm
Ca stock solution were added to separate, 100 ml volumetric
flasks and diluted to the 100 ml mark with doubly-distilled
water. Duplicate magnesium standards vere prepared with
concentrations of 0.2, 0.5 and 0.7 ppm. Duplicate calcium
standards vere prepared with concentrations of 2.0, 5.0 and
7.0 ppm. All final standard solutions contained 54 KC1
solution and 154 La solution by volume.
42
Approximately 0.8 kg of reference standard was prepared
from the tips of three large coralline algal heads collected
at the same site at French Frigate Shoals, Northwestern
Hawaiian Islands. The tips were placed in a heavy duty
plastic bag and gradually comminuted to smaller and smaller
pieces with a hammer. The bag was shaken and turned
regularly to mix the coralline algal fragments between bouts
of smashing. This procedure was continued until the grain
size approached that of coarse sand. The final powdered
form of the reference standard was obtained with a rock
pulverizer and placed in a large jar for additional mixing.
The composition of the standard determined by average daily
atomic absorption spectrophotometric analyses was 21.5
mole 4 MgC03 S.E. 0.06, n 50! ~ Reference standards were
prepared in an identical manner to the samples and analysed
during every AA session. All sample analyses were
normalized to the reference standard.
Magnesium and Calcium Analysis by Atomic Absorption
Spectroscopy:
Standard operating conditions for the analysis of
coralline algal calcite using a Perkin-Elmer Model 805
atomic absorption spectophotometer vere as follows: 1!
air/acetylene flame, 2! oxidant pressure: 30 psig, oxidant
flow: 50; fuel pressure: 8 psi, fuel flow: 30; 3!
wavelength: magnesium:UV-285, calcium:VZS-211, 4! slit 4, 5!
Ca-Mg tube with operating current : 15 ma, 6! flow spoiler,
43
7! aspiration rate: 4 ml min , 8! read time: 10 seconds, 9!
read delay: 6 seconds, 10! integration time: 8 seconds, ll!
10 cm burner head, single slot.
Magnesium concentration was determined to within +
0.001 ppm with a 2.5 scale expansion. Calcium concentration
was determined to within + 0.01 ppm with the same scale
expansion. The magnesium content from each treatment was
determined by analysing 2 tips/plant, 10 plants/treatment.
Each tip was analysed twice with a 24 error in precision.
The mean magnesium content is reported as mole 4 MgCO3 +
standard error S.E., n 20! where:
Mg ppm!/24.312X 100 'MOLE 4 MgC03
Mg ppm!/24.312 + Ca ppm!/40.08
RESULTS
Zn this section, correlations between various
environmental factors are presented. A summary of these
data is presented in Appendix I.
QRCEZH
Solar Radiation:
h
range of light regimes decreasing only at the lowest light
levels Figure 8!. An average growth rate of 1.55 mm/month
was measured between 1004 and 30% of ambient solar
laI1ILallight intensity. Arrow indicates "ambient" light conditions�34 of surface illumination! for all microcosm experiments.This light intensity is approximately equivalent to theintensity measured on reef flats in Kaneohe Bay at a depthof 3 meters. The key to all experiments below!, lists theexperiment number, the time period and duration of theexperiment, the graphic symbol associated with eachexperiment, and in three cases, the average daily solar
radiation Langleys! recorded during the experiment
KEY TO ALL EXPERIMENTS:
EXPERIMENT I: NOV-DECiEXPERIMENT II: JAN-FEB,EXPERIMENT III: APR-MAY,EXPERIMENT ZV: JUNE,EXPERIMENT V: JUL-AUG,
1983 i 231984; 211984 p 21
1984 i 201984 t 17
DAYS TOTAL ~ TRIANGLESDAYS TOTAL; CIRCLES; 310DAYS TOTALS SQUARESr431DAYS TOTAL; CROSSES;432DAYS TOTAL; DIAMONDS
0 0
O
O
ev o co
O 00 ao 4
4> "o~/~w j 3lb'8 HLMOg9
radiation. A 244 decrease in growth rate was measured
between 30% and 74 of ambient solar radiation. Growth may
have been inhibited at high �00%! light intensities in
Experiment XV which was conducted during the summer when
incoming solar radiation is a a maximum. Changes in the
p t }} ~ ' }}y
after one week of the experiment. Coralline algal tips from
the field collection site and "control" �34 of surface
illumination! light treatment were typically light pink in
coLor. Algal tips were deep red-purple after one week of
growth in the Low light treatment and yellowish pink in the
high light treatment.
Temperature:
Growth rate was relatively constant between 23o and
28.5 C Figure 9!. A gradual decrease in growth rate was
observed at temperatures less than 23 C. Growth rate
decreased rapidly at temperatures above 28.5 C + 0.5 C!.
In Experiment III, growth at 30 C was reduced by 504 over
} t ~}
exposed to a temperature of 32 C for less than one hour
resulted in death. No visually discernable difference in
pigment content was observed in any temperature treatment.
Calcite Saturation State:
Growth rate was linearly and positively correlated with
47
FlGURE 9. Growthtemperatures. Bartemperature in
experiments. See
1 Potallt sgguutj tindicates average seasonal variation in
"ambient" growth conditions for allkey to experiments in figure caption 8
48
C4
C! e! W ~ Cv C! aO
a o
s»o~s~~! sjvs Hieozo49
calcite saturation state Figure 10!. A two-fold increase
in grovth rate was measured between 100% and 8004 calcite
saturation. Coralline algal tips vere yellowish pink at low
�004 and 2354! saturation states. The least scpzares fit to
the data from all experiments conducted during the period of
one year is:
MEAN GROWTH RATE mm/month!
0. 97 + 0 ~ 0012 � CALCXTE SATURATION! l
0.90, n~l5.
The settlement of coralline crusts on the plexiglas sides of
the microcosms was dependent on the carbonate saturation
Average coralline crust settlement was 5.0 crustsstate.
m d n 2, S.D.~7.0! at a saturation state of 235 4,
144.0 and 133.0 crusts m d n 2, S.D. 39.0 and 30.0,
respectively! at saturation states of 450 4 and 750
respectively.
Temperature:
An increase in magnesium content was measured, with
increasing temperature between 19.5 and 30 C Figure 12!.
50
Solar Radiation:
Magnesium content did not vary systematically with
different light intensities Figure ll!. The total
variation in magnesium content for all light experiments was
17.5 to 18.5 mole 4 MgCO3.
f ECl1JL5calcite saturation states. Bar indicates average measuredrange in calcite saturation state for "ambient" grovthconditions for all experiments. See key to experiments
in figure caption 8
COC!
OC!
043
CO0
0 QO Q Q + Q gp
R~"~~/~~ j 3lb'8 Hl/AQHQ
O O O 0C4
g ~ K Mglggn ~as a function of light intensity. See key to experiments in
figure caption 8
53
C!
OO
~03 ~W 'X 31ONI
COCO
O OC!
O
EggllC1at different temperatures. See key to experiments in figure
caption 8
03<W 4 3 ION56
The total range in magnesium content among all temperature
experiments was about 16 to 19 mole O' MgCO3. The least
squares fit to data from all experiments conducted at
different seasons over the period of one year is
mole 4 MgC03 ~ 11.3 + 0.26 T C,
r 0.81, n 12.
This relationship may be curvilinear. A quadratic fit
to the data, however, did not explain statistically, a
significant p < 0.05! portion of the variablity in
magnesium content.
Calcite Saturation State
Magnesium content was positively correlated with
calcite saturation state SS; Figure 13!. The total range
in magnesium content among all calcite saturation state
experiments was about 15.5 to 19.5 mole 4 MgCO3. The
quadratic function, determined as the best fit for data from
all experiments conducted at different seasons over the
period of one year, is:
mole 4 MgC03 ~ 14.76 + 0.01 SS - 6.6 x 10 SS
r ~ 0.85, n=15.
Saturometry experiments revealed that the ambient reef
water was undersaturated with respect to coralline algal
powder with about 18 mole 0 MgC03 Table 3!. A. decrease in
pH indicates precipitation implying supersaturation!, an
grown at different calcite saturation states. See key toexperiments in figure caption 8
o
o o 0U
O
O
TABLE 3. Change in pH of seawater samples after the additionof carbonate minerals. Positive and negative pH changesindicate undersaturation and supersaturation, respectively,
with respect to the powder added
�8 MOLE 4 MgCO3!
325 490 755 1, 641
7.99 7.81 7.63 7.32
pH
pH difference
CALCITE POWDER
pH
pH difference
60
Calcite Saturation State �!
-log ZAP CaCO3!
before
after
before
after
8. 03 8. 22 8. 43 8. 86
8. 11 8. 25 8.44 8. 85
+0.08 +0.03 +0.01 -0.01
8.02 8.22 8 ' 41
7.99 8.19 8 29
-0.03 -0.03 -0.12
increase in pH, dissolution hence apparent
undersaturation!, as demonstrated by : CaCO> + H Ca +
HCO3 , where Mg can be substituted for Ca . Unlike
calculated values for carbonate saturation state, this
direct saturometry method measures saturation state with
respect to the powder not the mineral! and measures the
effects of fine-grained particles and strained surfaces
Chave and Schmalz, 1966! as well as a range of Mg +
contents. Thus in the upper part of the table it can be
dd th 1 1th p
being measured rather than with respect to 18 mole
magnesian calcite. Saturation state and -log ZAP are
included for comparison and were calculated from pH and,
alkalinity, at 25o C and 35 per mil salinity. Carbonate
saturation state is given with respect to calcite using the
ksp for calcite from Plath et al. �979!. The -logZAP CaC03! was calculated according to Wollast et al. �980!
in which y Ca ! x y CO ! ~ 10 m Ca ! ~ 10
and m CO3 ! 0.351 x 10 ; all values are given in
moles/kg SW!, and calculated from measured values of pH and
alkalinity. Seawater was undersaturated with respect to
alal11 " ' f ~ � w
7.62.
All seawater treatments used in the microcosm growth
studies were supersaturated with respect to calcite powder
and undersaturated at least up to a pH of 8.4 and -log
61
FIGURE 14. Change in calcite saturation state of seawaterover a 24 hour period on a windward reef flat in KaneoheBay, Hawaii. Estimated magnesian calcite saturation atdifferent magnesium contents from Schoonmaker, 1981! are
also given
62
O O O O O OO O O O
%! 3LVLS NOILVHALb'S 3LI!lb'!
63
range in seawater pH tested is similar to the range measured
over the reef flat in Kaneohe Bay. The reef flat in Kaneohe
Bay experienced daily fluctuations in calcite saturation
state Figure 14!. Magnesian calcite saturation with
respect to magnesian calcites containing 12 mole 4 MgCO3 and
14 mo1% MgCO3 from Schoonmaker, 1981! is indicated in
Figure 14 '
DISCUSSION
MAGNES1UM C01PZZ2PZ:
Previous investigators have never measured
simultaneously, growth rate and magnesium content. Moberly
�968! correlated changes in skeletal growth patterns with
changes in magnesium content. Kolesar �973! used growth
rate values reported in the literature and correlated
magnesium content with reported periods of slow and rapid
This investigation represents the firstgrowth.
experimental test of the biological-kinetic versus physical-
chemical hypothesis in which magnesium content, growth rate
and physical-chemical factors were measured simultaneously
in individual experiments'
The experimental results of the present study suggest
g t ~ ' ' 1
influenced by growth rate, but is primarily changed by
environmental factors of a physico-chemical nature. The
evidence supporting this conclusion is exemplified by the
following trends: 1! changes in growth rate without changes
in magnesium content, 2! changes in magnesium content
without changes in growth rate, 3! identification of a
single relationship describing the magnesium content of many
groups of calcitic organisms as a function of physico-
chemical factors.
Light experiments do not support the growth rate
hypothesis. Changes in light intensity were assumed to have
no impact on the physical or chemical properties of seawater
such that magnesium content would be a function of growth
rate alone. Magnesium content of the algae remained constant
despite a decreased growth rate at low light levels.
Temperature experiments do not support the growth rata
hypothesis. Experimental data can be used to describe a
linear relationship between magnesium content and
temperature whereas the relationship between growth rate and
temperature was curvilinear. Growth rate decreased with
increasing temperature without a concomitant decrease in
magnesium content. Conversely, magnesium content decreased
with decreasing temperature with little change in growth
rata. Kolasar �973! concluded that magnesium content was
influenced primarily by growth rate because he correlated
slow growth during warm summer months with a constant, high
magnesium content, and rapid growth during winter months,
with low magnesium content and water temperature. He did
65
not measure growth rate in his experiments and assumed that
the growth rates measured by Johansen and Austin �.970! for
p ' f tt
p. p tt
location. Kolesar did not find a correlation between
magnesium content and temperature in his laboratory
experiments and concluded that growth rate was the primary
factor influencing magnesium content. He did not really
provide evidence in support of the growth rate hypothesis,
because he did not measure the growth rate of laboratory
grown coralline algae at different temperatures. A re-
interpretation of his field measurements based on the
conclusions formulated from experiments conducted in the
present investigation suggests that when the temperature
regime in the natural environment exceeds optimal conditions
for growth, growth rate decreases without a reduction in
magnesium content.
A physico-chemical control of magnesium content is
further suggested by the overall remarkable similarity in
equations describing the relationship between magnesium
content and temperature in seven genera of coralline algae
and three classes of benthic invertebrates Table 4!, For
these organisms, magnesium content was correlated with
seawater temperature at the time of collection. The
magnesium content measured by Chave �954! for calcareous
algae, echinoids and. foraminifera was correlated with
66
TABLE 4 ~ Magnesium content as a function of temperature oC!: A! Agegian, this study, algae experimentally grownat different seawater temperatures, magnesium contentdetermined by atomic absorption spectroscopy, r 0.81, n 12.
~ < I F 1d~a ~ made during a single season, at one location inMaine, but at different depths down to 40 m. Magnesiumcontent determined by elec!ron microprobe correlated withcollection temperature, r ~0.88 n 5. C! Kolesar �973!,field collections made seasonally at one location, SantaCatalina, California. Magnesium content determined by atomicabsorption specposcopy was correlated with collectiontemperature, r 0.84-0. 93, n ~ 7-9. D! Chave �954!,magnesium content determined by x-ray diffraction correlatedwith collection temperature. E! Chave �954! magnesiumcontent determined by x-ray diffraction correlated with
average annual temperature
~ COlllll ~ ~
alaaeu
Cmllllm
euexl �" KDLcu-
EllillUn ~
67
asteroids
ophiuroids
crinoids
coralline algae
echinoids
echinoid spines
foraminifera
MOLE 0 MgCO3 ~ 8.6 + 0 ' 26 T C!
MOLE 4 MgCO3 ~ 9.0 + 0.24 T C!
MOLE 4 MgCO3 ~ 9.7 + 0 ' 25 T C!
MOLE 4 MgCO3 ~ 10.6 + 0.29 T D!
MOLE 4 MgC03 ~ ll e0 + 0 ~ 28 T D!
MOLE 4 MgC03 ~ 10.2 + 0.22 T D!
MOLE 4 MgC03 sm 6.8 + 0.68 T E!
MOLE 4 MgC03 ~ 6.1 + 0.32 T E!
MOLE 4 MgC03 ~ 3.6 + 0.23 T E!
MOLE 4 MgCO3 ~ 3.4 + 0.48 'T E!
average annual temperatures. In these examples, the
magnesium content may not reflect the average annual
temperature but a temperature maximum or minimum!
coinciding with the time of collection. The lack of
similarity between these organisms and those described above
might be predicted, in part, if the relationship between
magnesium content and annual average temperatures was made
for geographic areas characterized by large extremes in
temperature.
A relationship between temperature and calcite
saturation state is implicit in the equations in Table 4;
however, biological factors, that are independent of
temperature, such as photosynthesis and respiration will
influence the calcite saturation state of seawater. The
degree of influence is dependent on the mass balance among
the metabolic reactions, the gas flux, and the local
hydrography Smith, 1985!. This investigation shows for the
first time, that the calcite saturation state of seawater
fl th K ~ ' dp
of temperature. Local variations in saturation state,
therefore, such as that measured on the reef flat in Kaneohe
Bay may be expected to influence magnesium content.
The growth rate hypothesis did not explain the adaptive
significance of magnesium in algal calcite. Under this
hypothesis, any variable that influences growth rate such as
light intensity a.g. Soegiarto, 1972!, water motion e.g.
68
Soegiarto, 1972!, herbivorous grazing e.g. Steneck, 1981:
Adey and Vassar,1975!, or nutrient concentrations e.g.
Kindig, 1977! should influence the magnesium content of
coralline algae. The demonstration that physico-chemical
g * * t l g I.
implies that magnesium is an important element in the
biogeochemical ecology of this species. The demonstration
that the solubility of magnesian calcites increases with
increased magnesium content Plummer and Mackenzie, l981;
Mucci and Morse, 1983; Walter, 1983! suggests that coralline
algae may respond to variable environmental conditions
through changes in magnesium content, and hence, skeletal
solubility.
Growth rate was reduced byof each experiment.
GROWTH:
Solar radiation is usually considered one of the most
important factors influencing plant growth in the sea. The
compensation light intensity for phytoplankton cells
usually about 14 of surface illumination! is the depth at
which photosynthetic gains ecpxal respiratory losses Parsons
et al., 1979!. Phytoplankton cells are exposed. to a variety
of light regimes as they are mixed. in the surface waters of
the ocean. Zn contrast, benthic macrophytes must adapt to a
particular set of environmental conditions. The phycobilin
Plg P ' ~ gd ' ll
the lowest light treatments within one week of the beginning
approximately 304 at lowest light intensities. The
ability of coralline algae to adapt to low light conditions
may in part explain recent findings that the deepest plant
life recorded �68 m! in the ocean is a coralline alga
Littler, et al., 1985!.
The experimental results indicate that the growth rate
t ~ 1lttl tl 'y fg K d~'
between 304 and 100% of surface- illumination. Coralline
algae have been reported from high light environments in
intertidal zones e.g. Taylor, 1950, Shepherd and Womersley,
1976; Saito et al.,1976! to extremely low light environments
such as caves Dellow and Cassie, 1955!, deep tropical
lagoons Gilmartin, 1973! and deep water slopes Littler et
al., 1985' Agegian and Abbott, 1985!. Individual tropical
coralline algal genera have been found from depths of 0 to
90 m Adey et al., 1982!, hence a wide range approximately
100 fold! in light conditions.
The growth of corals and many other tropical organisms
is typically limited within a relatively narrow temperature
range Figure 6; Jokiel and Coles,1977; Houck et al., 1977!.
p th g h ~ ~ ~
most dramatic at only a few degrees higher than ambient �9-
30 C!, a characteristic response for tropical marine
organisms living near their lethal limits. Growth rate was
fairly constant between 23 and 28.5 C, then decreased by
approximately 304 at 19.5 CD A related finding, reported
70
by Littler �971!, was that the photosynthetic rate of
onkodes was constant at 24 and 27 C.
t tth ~
m Adey et al., 1982!, and yet it was capable of
considerable growth at light and temperature regimes
characteristic at, depths of 80-100 m in the Hawaiian
Archipelago.
Saturometry experiments revealed that surface seawater
with a range in pH values was undersaturated with respect to
d athS 1 1 g
f ~ t d d l.th
respect to its non-living skeleton. Lower than ambient
calcite saturation state resulted in decreased growth and
magnesium content in this species as well as reduced
settlement of coralline crusts on artificial substrata at
235 4 calcite saturation. These observations suggest that
CO32 ion concentration may limit the growth and settlement~h. l ~ 1 ~ 1 ~ ~ ~ 1 ~ ~ ly
calcite saturation state.
The effects of pH and hence seawater saturation
state! on the growth of coralline algae have been described
by two other investigators. The results of the present
study are different from those of Smith and Roth �979! and
Borowitzka �981!. The range in calcite saturation state
used in this study �00%-860 0! was approximately equivalent
to pH values between 7.5 and 8.5 Table 3!. Over a similar
71
range in pH � ~ 5-8.3! Smith and Roth �979! documented an
increase in the calcification rate of the articulated
1g, ~~, 'the egg
hence saturation state. Smith and Roth �979! altered
seawater pH by bubbling in CO2 gas and therefore changed the
total carbon c.ontent of seawater. Increased carbon content,
of seawater independent of saturation state may stimulate
calcification in coralline algae. The effects of increased
th g
investigated in the present study. For this reason, these
results are not directly comparable to the results presented
in this study. In addition, their results are difficult to
interpret because the "ambient" seawater specific
alkalinity i.e. ratio of alkalinity to chlorinity! reported
by Smith and Rath �979! was approximately 604 higher than
that measured in average surface seawater. Borowitzka
�981! found no difference in the calcification rate of the
articulated coralline alga, ~~h'~ ~o~a,i~, at pH values
of 7.0 and 8.3; he observed a decrease at pH 9.0. He
altered seawater pH with acid HCl! and base NaOH!, as was
done in the present study. Differences in methodology may
explain part of the discrepancies. Borowitzka �981! used
14C to measure photosynthesis and calcification. His
experiments were relatively short-term hours! in comparison
to the long-term experiments weeks! conducted in this
investigation. Experimental results based on short-term
72
experiments are often extremely variable e.g. Goreau,
1963! ~
Daily variations in calcite saturation state influenced
by photosynthesis and respiration may influence the growth
and settlement of coralline algae within particular reef
environments. Variations in calcite saturation state within
specific communities are dependent on the balance between
organic processes that take up carbon, e.g. photosynthesis,
and processes that release carbon, e.g. respiration. This
balance is mediated, by the residence time of seawater
flowing over a particular community. Zn shallow water
reef systems, luxuriant coralline algal growth generally
occurs on windward reef flats see review by Johansen, 1981!
where turf algae and corals may also be present. Many
of these reef flats are characterized by net organic carbon
production Gladfleter and Xinsey, 1985!, P � R, where P
equals organic carbon fixation and R equals respiration.
The P/R ratio may be used as an indicator of which process
photosynthesis or respiration is predominant within a
community, For instance, P/R of a windward reef flat at
French Frigate Shoals, Hawaii Grigg, 1985! was about 1.77
indicating an excess carbon fixation over respiration. Zn
contrast, lagoons and coral knolls within lagoons had a P/R
ratio close to 1.0 indicating no net carbon production.
Kinsey and Gladefelter �985! and Kinsey �983! summarized
the P/R ratios for various biotopes in coral reef
73
environments. Algal dominated biotopes were chazacterized
by an average ratio of 2.12, sand and cozal dominated
biotopes were characterized by a ratio of 0.99. High
carbonate saturation state would result from communities
characterized by a high P/R ratio and a seawater residence
time long enough to build up the signal Smith, 1985!. Xf
most surface seawater is undersaturated with respect to
magnesian calcites with 14-l8 mole 4 MgCO3 Schoonmaker,
1981; Walter, 1983!, the abundance of coralline algae in
specific habitats might be explained, in part, by enhanced
growth and settlement of spozes at increased seawater
saturation states chazacteristic of predominantly
photosynthetic communities.
BEOGEOCHZMZCAL CYCLES AND CORALLINE ALGAE: Past and Future
Some predicted effects of a doubling of atmospheric CO2
concentration from anthropogenic sources! on the ocean
reservoir include a 0.5 unit decrease in sea surface pH and
hence decreased seawater satuzation state! and a mean
increase in sea surface temperature of 2 to 3 C e.g.
Qlson, 1982!. This study indicates that the growth of
state of seawatez and temperature. The results of these
experiments suggest that the biogenic deposition of
magnesian calcite in subtropical seawater may be reduced by
approximately 604 if the C02 in the atmosphere doubles.
74
Microcosm studies have provided the first experimental
evidence that the magnesium content of coralline algae is
the result of a physico-chemical process not strongly
mediated by growth rate.
The physico-chemical relationship between the magnesium
h ti fcontent of
and calcite saturation state is summarized by trend surface
analysis in Figure l5 using the SAS Statistical Analysis
System! general linear model multiple regression program.
This model was run initially with all variables and
interactions between variables. Only statistically
significant variables p < 0.05! were retained in the model.
Although calcite saturation state can be function of
temperature, calcite saturation state is also influenced by
biological processes independent of temperature. The
retention of both of these variables in the final equation
indicates they both explain a significant amount of
independent variability in magnesium content. In addition,
the experimental data show that magnesium content may be
influenced by calcite saturation state, independent of any
changes in temperature. The following empirically derived
model is given {with standard errors, sbn, for each
coefficient! as a general summary of the effects of these
FIGURE 1S. Surface trend analysis showing the magnesium't" ' ~~~ ~ as a function of temperature
and calcite saturation state determined from microcosmexperiments
O
LP!C4
CKUJCL
P! I�
0 g 0 0 00 ~ 0 0 0
P!
'L! 3''lS NQll48Plb'5 3ll3lb'3
77
MOLZ 4 MgC03» 0. Ol SS! - 6 ~ 0 x lO SS!
l. 62 T! -0. 028 T! - 8 o 25
n» 27; r 0.89;
-6. ~ 3sbl 0 ~ 0017' sb2»1 ~ 68 x 10 t sb3 0 ~ 486'' sb4 9 ~ 7 x 10 ~
Calcite saturation state accounted for over two thirds
�5 4! of the total variation in magnesium content of
y l.
physical relationships described by this model suggest that
an average decrease of 0.5 mole 4 MgCO3 would be predicted
for temperature and saturation state conditions resulting
from a doubling of atmospheric CO2.
Although the importance of CO2 in global biogeochemical
cycles has been recognized for many years Arrhenius, 1896;
Chamberlain, 1898!, and the increase in atmospheric C02
owing to anthropogenic sources documented see Brewer,
1983!, the potentially substantial variations in atmospheric
C02 concentration over a geologic time scale have only
recently been re-emphasized Sandberg, 1983; Mackenzie and
Pigott, 1981; Berner, et al., 1983; Neftel, 1983!. Large-
scale fluctuations of atmospheric CO2 may have occurred over
10-100 million year oscillations in conjunction with changes
in tectonic activity. For example, Mackenzie and Pigott
�981! postulated that the submergent mode of active plate
convergence, obduction and subduction of sediments, large
ridge volume and high sea level gave rise to low erosion and
sedimentation rates, less restricted environments of
78
Pigott, 1979; Wilkinson, 1979!. The appearence of the
Corallinaceae during the Pennsylvanian and Permian, their
79
carbonate deposition, and relatively high atmospheric CO2
levels, These changes stem from an increased rate of
production of CO2 from diagenetic and metamorphic reactions
at subduction zones. Berner et al. �983! constructed a
computer model that considers the effects of continental
weathezing of carbonate and silicate minerals, precipitation
of calcium carbonate, and metamorphic-magmatic decarbonation
of carbonate minerals as a consequence of plate subduction
on atmospheric C02 concentration. Depending on the
spreading rate used in the model, calculated atmospheric CO2
values ranged between 3 and 100 times the present
atmospheric value of 345 ppm. Periods of high atmospheric
CO2 concentration may have resulted in "Calcite Seas"
Milliken and Pigott, 1977; Wilkinson, 1982!, a seawater
with a saturation state favoring the deposition of calcite
over more soluble phases such as aragonite. Two periods of
time during the Phanerozoic of low atmospheric CO> were the
mid-Carboniferous to late Tz'iassic, and the early Cenozoic
to the present. These periodic oscillations were described
by changes in the inferred carbonate mineralogy of ooids
Sandherg, 1983! and correlated with tectonically induced
climatic events.
Variations in ocean chemistry through the Phanerozoic
may have influenced the mineralogy of calcareous organisms
FIGURE 16. Inferred oscillations in non-skeletal carbonatemineralogy about an aragonite threshold from Sandberg,1983!. Comparisons are made to sea level curves, climaticepisodes from Sandberg, 1983! and, the evolution of theSolenopozaceae proposed calcareous red algae!, theCorallinaceae and various herbivore groups
from Steneck, 1982!
80
I 10SPECIES
V Z
0
I> oJL'4V»o VIX ~ IO
ul
o
0 0U IJI
UJ 4<Z4
Z»g~M UJ QUJ VIowe
Vl
UJ
0
»IJJ»0O<z~~
OOg
81
PC CAhh, OROI SIl. DEV. CARB PER, TR, JUR. CRET. CEN
ICEH SE GREENHOUSE ICEHOUSE GREENHOUSE ICE
PC CAhh. ORC4 SIL. DEV. CARB. PER. TR. JUR. CRET. CEN.
ICE HOUSE GREENHOUSE ICE HOUSE GREEN HOUS E ICE
I
O 0 ~ U'U
V
apparent disappearance during the Triassic, and radiative
explosion at the beginning of the Cenozoic Figure 16! is
consistent with the trends described by Sandberg �983!.
The species diversity of coralline algae reported for the
late Paleozoic is low Steneck, 1983!. Coralline algal
abundance, however, was apparently high owing to a single
genus, chaeolitho h 1 u Wray, 1964!. This genus is very
similar morphologically to the Recent coralline alga,
Johnson, 1963!. These leaflike algal remains
are generally considered to be widespread and abundant
throughout marine strata of Pennsylvanian and early Permian
age Wray, 1964!. The early Cenozoic was characterized
by an evolutionary explosion of coralline alga species. A
similar radiative explosion, which has continued to the
present, occurred in hermatygic corals during the late
Triassic Stanley, 1981!. Therefore, it would appear that
the "aragonite threshold" described by Sandberg �983! might
be better described as a "magnesian calcite threshold".
82
III ~ THE MAINTENANCE OF STANDARD REEF PERFORMANCEBY CORALLINE ALGAE IN THE HAWAIIAN ARCHIPELAGO
INTRODUCTION
Chemical estimation techniques alkalinity depression!
have been used to estimate rates associated with specific
biogeomorphological zones on individual reefs from widely
scattered areas. see reviews by Gladefelter and Kinsey,
1985 and Kinsey, 1983!. High calcification activity is
characteristic of fringing reefs, algal ridges and atoll
margins. Low calcification activity is commonly measured in
lagoons or areas in which sediments accumulate. The
activity rates measured in these environments are, for the
most part, similar between reefs despite differences in
geographic locations. Smith and Kinsey �976!, Kinsey
�983; 1978! and Smith, �978; 1983! considered this
phenomenon as describing a standard reef performance.
Standard reef performance has been estimated at the
ecosystem level Smith, 1978; modified slightly by Smith,
1983!. The bimodal activity described by Smith �978!
estimates that 954 of the reef calcifies at a slow rate,
such as in lagoonal environments, of 800 grams CaCO3m y
and the remaining 54 at 4000 grams CaCO> m y such as at
reef perimeters. Considering the reef ecosystem as a whole,
the standard reef performance calculated from these figures
is about 1.0 x 10 grams CaCO> m y . Defined in this
83
manner, standard reef performance on an ecosystem level!
can be considered a measure of the biog~omorphological
development of the reef ecosystem since the last low stand
of sea level 9,000 -11,000 years B.P!.
Biological estimation techniques of carbonate
production have been used to identify latitudinal variations
in coral growth Grigg, 1982! in the Hawaiian Archipelago.
Xn this chapter two questions are addressed: 1! Zs there a
standard reef ecosystem performance on reefs in the Hawaiian
Archipelago'P 2! If so, how is standard reef performance
maintained along latitudinal gradients in environmental
factors7
METHODS
Shallow Water Reef Area:
I defined "shallow water reef area" m2! as the area
between 0-20 m on U.S. Coast and Geodetic Survey Charts
along the Archipelago from Hawaii to Kure Atoll �9o-30o N.
latitude!. The locations of the reefs included in this
investigation are shown in Figure 17. The map area was
determined by tracing from this chart onto a transperant
grid sheet and counting the squares. The smallest delimited
area was approximately 4 x 10 m . These shallow reef areas
excluded emergent island areas.
Total shallow water reef area was subdivided into three
biogeomorphological zones: RXDGZ, REEF and SEDZMENT Table
5!. The percent of total shallow water area in each zone was
FZGURZ 17. Map of the Hawaiian Archipelago. Dotted linesshow approximate position of the 100 m bathymetric contour
85
Oz0lf!C4
86
TOTAL AREASXTE LATITUDE SHALLOW WATER REEF AREA
N! � RXDGE! � REEF! � SEDIMENT! x 10 m !
80 51KURE 28 ~ 4
MZDW 28.3
P+H 27.9
LZS 26 ' 0
LAYS 25 ' 7
NARO 25 ' 4
GARD 25.0
FFS 23.7
NECK 23.5
NZHO 23.0
OAHU 21 ~ 0
NAUZ 20.7
HAWA 19.3
8679
37425 5520
27937 55
4046
37612 30
50
45120 25 55
50 50
50
14270 25
80 19 18
80 19
87
TABLE 5. Percentages of ridge, reef and sediment zones onindividual reefs �! and total reef area x 10 e !
determined by synthesizing 1! zonal areal determinations
from charts, 2! personal field observations on all reefs
northwest of the island of Kaula, in addition to many reefs
around the main Hawaiian Islands, and 3! zonal areal
determinations and percent cover of corals and coralline
algae from the literature Dana, 1970; Gross et al.,1969;
Littler, 1973a; 1973b; Brook and Chamberlain, 1967; Dollar,
1982!.
The RIDGE zone is defined as the area < 2 m in depth
dominated by hard substratum and covered almost exclusively
by branched and encrusting coralline algae. RIDGES include
long, narrow structures subdividing lagoons, reef perimeters
Northwestern Hawaiian Islands! or f ringing reef main
Hawaiian Islands!. The REEF area is characterized as
predominantly hard substratum within a 2-20 m depth range
dominated by the coral genus ~~e and coralline algal
crusts. SEDIMENT zones are distinguished from the other two
zones as areas between 2-20 m, with significant sediment
accumulation. These areas are not included in carbonate
production estimates. SEDIMENT areas around high islands
refer primarily to the deep areas around the bases of coral
reefs where sediment and rubble accumulate, and sediment
dominated areas on reef flats behind fringing reefs, The
SEDIMENT zone at all other sites includes these areas in
addition to sediment dominated areas enclosed by reefs i.e.
lagoons!.
88
Carbonate Production:
The predominant species of calcareous organisms on
these reefs are corals of the genus p~o '~ Grigg, 1982!
g th I ~h d ~l
Littler, 1971!. These dominant genera represent three
morphological types, branched coralline algae, encrusting
coralline algae and lobate forms of corals.
Carbonate production by encrusting coralline algae used
in calculations for RIDGE and REEF areas was determined at,
French Frigate Shoals at a depth of 2 m by long-term �83
days} settling plate experiments. Pieces of coralline crust
were removed from settling plates. Carbonate production of
crusts was determined by weighing pieces of crust and
measuring the surface area of the crust. Carbonate
production by coralline algal crusts Table 6! was then
calculated as:
CRUSTAL WEIGHT grams! X PERCENT LIVING COVER / CRUSTAL AREA
cm ! X LENGTH OF TINE ZN THE FIELD days!.
The growth rate of the branched coralline alga,
I. ' ~
French Frigate Shoals and Kure Atoll by ~ ~sit growth
experiments Chapter I!. Carbonate production by branched
coralline algae was determined as:
89
TABLE 6. Average carbonate production by coralline algalcrusts on RIDGE area of French Frigate Shoals determinedfrom measurements of crust. area and crust weight as
described in the text
CARBONATE PRODUCTIONCRUST WEIGHTCRUST AREA
grams cm y ! cm ! gr~s!
AVERAGE CARBONATE PRODUCTION S.E N
g cm y !
2.1 x 10 400 200. 206
90
4.456.35
5.40
6 ' 10
2 ' 60
6.75
5.80
4.40
4.50
3.70
3.05
1.65
4.35
4.00
5.35
4.35
7.10
2.00
2.00
1.90
1.494
l. 661
1.734
1.7670.624
2.527
2.0991. 533
1.722
1.522
1.241
0.808
1.878
1.904
1 ~ 768
1.307
2.775
1.055
0.958
1. 024
0. 179
0. 140
0. 172
0. 155
0 ~ 1280.200
0.193
0.186
0.204
0.220
0.217
0.262
0.231
0.254
0.177
0.161
0.209
0.282
0.256
0.288
~ ""''s p'"'""~d * *1 I gdifferent locations. An average skeletal density of1.56 g cm Steam et al., 1977! vas used in all
calculations
MEAN GROWTH RATE
~y !
FFS
2.0 x 10
91
12.4
12.0
14.7
CaCO> PRODUCTION
gm y !
2.0 x 104
1.9 K 104
2.3 x 10
GROWTH RATE {cm y, Table 7! x AVERAGE SKELETAL DENSITY
�.56 g cm , from Steam et al.,1977! x PERCENT LIVING
COVER IN THE RIDGE ZONE Table 8! ~
Carbonate production by corals on REEF areas was based
on the production of ~po '~t ~obata according to the
empirically determined relationship from Grigg, in which Y
44.9-1.39 X! where Y kg CaC03 m y and X latitude
N.!. Total coral ccver reported by Grigg �982! was high,
because his transects were conducted at 10 m depth on
leeward reefs in areas of maximum coral cover. These areas
represent a fairly small fraction of the total shallow water
area. I attempted to obtain a more representive estimate of
percent cover for the reef ecosystem by calculating the mean
coral cover determined from 10 different sites Grigg, 1982,
Dollar, 1981! off the leeward western! half of the island
of Hawaii. This average was approximately 46 4 of the
percent cover reported by Grigg. I assumed that for the
most. part, coral cover on the windward eastern! half of the
island was insignificant owing to rough sea conditions and
freshwater runoff. Therefore, the percent cover estimate
used for coral cover on REEF zones {Table 8! at all sites
represents 234 of the cover reported by Grigg {1982!.
Percent Living Cover:
< '"e
92
TABLE 8. Percentages of living cover of coralline algae andoorals within different zones
LIVING COVER �!
COHJKLINE ALGAE CORALS
CRUST HEAD
REEFREEFRIDGEZONE
1020
MIDW 20 lo
P+H 2850
35LIS
50 42
MARO 1431
30
l43550FFS
40
NIHO 40
40 35
16MAUI
20HAWA
93
ORGANSISM
MORPHOLOGY CRUST
RIDGE
Table 8! was estimated from five, 10 m long random
transec's on the windward ridges of Kure Atoll and French
Frigate Shoals. Percent cover was determined from 50
sampling points on each transect at 20 cm intervals, and
calculated as the number of "hits" points falling on a
given species! divided by the total number of points
sampled on each transect n 50!. Averages are reported for 5
SCILK! and
coralline crusts on Oahu was t .en from the literature
Littler, 1973, 1985!. Qualitative estimates of percent
cover were made visually at, Pearl and Hermes Reef,
Lisianski, Laysan IsLand, Maro Reef, Gardner Pinnacle,
Maui, and Hawaii by snorkeling over RIDGES throughout these
reefs.
Average percent cover of coralline algae on REEF areas
was estimated from 10 m long random transects at a depth of 10
m on all islands except Hawaii. Coralline REEF cover
determined on Maui was applied to Hawaii. Percent cover was
determined from a total of 100 points per transect. Average
percent cover is reported for Lisianski � transects!, Maro
Reef � transects!, and French Frigate Shoals � transects!.
One transect was conducted at all other REEF sites. The
estimated coralline crust cover for Oahu represents an
average between the literature values of Littler �973! and
one transect conducted on the windward side of the island.
RESULTS
Carbonate production by encrusting coralline algae was
2.1 x 10 g m y Table 6!. Changes in carbonate
production by encrusting coralline algae with depth vere not
measured. Experimental evidence suggests that depth-related
changes in light intensity do not significantly alter the
~ f
illumination Chapter II! and it is assumed that the crusts
behave in the same manner. The estimated carbonate
production by coralline algal crusts at French Frigate
Shoals, therefore, was used on RIDGE and REEF areas at
different latitudes. The carbonate production by the
I HzCtgl1b
oui' . d ~ ~~
A eo ' am ! measured by Sogeiarto �972! on
fringing reefs off Oahu was similar between species, 3.6
x 10 g CaCO> m y . The carbonate production estimate
used in this study for crustose coralline algae is low in
comparison to other values reported from tropical and
subtropical locations Sogierarto, 1972; Steneck and Adey,
19'76! .
2- CM!balll measured on Kure Atoll,
French Frigate Shoals and Oahu was similar and did not vary
systematically with latitude; therefore, an average
carbonate production, 2.0 x 10 g m y , was used in all
calculations Table 7!.
95
Littler �971! found that the branched coralline alga
k l
kk»' ~ '"' l ' "' '"d'"d
f ff 'klkl. k ., . k~
observed to be abundant on reefs in the Northwestern
Hawaiian Islands north of Kauai!. Other species of
d * ill ld
kddkkkk ~ ~ ~ ~ ~ "- "'f
sporadically within the RZEP zone < 0.5 0! and are not
included in the carbonate production estimates for this
zona.
DISCUSSION
Bi.ogeomorphological Classification of Hawaiian Reefs:
Hawaiian reefs are biogeomorphologically diverse. Six
types of reefs Table 9! were identified based on the
presence or absence of lagoons and basalt. Reefs growing on
volcanic basements of different ages have been combined into
the sama reef type in some cases, however, overall the age
of the volcanic basements increases from type 1 to type 6.
Type 1 reefs are associated with young, high volcanic
islands. Vertical growth by corals is primarily responsible
for the production of calcium carbonate Table 10!. RIDGZ
areas are poorly developed. Estimated total carbonate
production on these reefs is high Figure 18! because
lagoonal environments low carbonate production areas! are,
for the most part, absent.
96
TABLE 9. Biogeomorphological summary of Hawaiian reefs
97
Type 2 reefs are associated with geologically older
basalt outcrops, remnants of original high islands. Ridges
and lagoons are absent in type 2 Hawaiian reefs. Reefs
growing at Nihoa and Neckers Islands are subject to rough,
open ocean sea conditions in absence of a protective ridge
structure.
French Frigate Shoals type 3! is the the only reef
possessing a basalt outcrop with extensive ridges and
multiple lagoons, The largest total shallow water area
occurs at French Frigate Shoals.
Hawaiian reefs without basalt remnants are classified
by "no lagoons" type 4!, "multiple lagoons" type 5! or
"single lagoons" type 6! developing from the oldest
volcanic platforms in the Hawaiian Archipelago.
Extensive ridges and multiple lagoons are found on Maro
Reef, Lisianski, and Pearl and Hermes. Ridge development at
Laysan Island was limited to a small fringing reef around.
the carbonate island itself. Lagoons are absent at Laysan.
Most of the shallow water reef area at Kure Atoll and
Midway Island is within single lagoons surrounded
peripherally by a ridge structure.
A model for Hawaiian reef biogenesis see Littler,
l985! schematically depicts the possible evolutionary
development of the biogeomorphological zones, REEF, RIDGE,
AND SEDIMENT, for type 1 reefs defined in this
investigation. The youngest stages of reef development
98
Hawaii! are characterized by vertical carbonate accretion
by corals in the REEF zone. The RIDGE zone is an irregular
feature that is not uniformly Developed around the youngest
high islands. The SEDINZNT zone is developed only at the
base of the REEF zone. As the RIDGE becomes more extensive
Oahu!, sediments accumulate on reef flats leeward of the
ridges fringing reefs!. Lagoonal and ridge structures
characteristic of mature atoll systems reef types 3 , 5,
and 6! are poorly developed.
Littler �985! explained this developmental model as a
eutrophication process influenced by nutrient enrichment
from "biological succession and soil development on the
reef's terrestrial watershed". Frondose algal development
might be explained by this model; however, considering reefs
less impacted by man types 2-6!, coralline algal abundance
both latitudinally and on specific reefs is correlated, in
general, with extremely nutrient-poor water.
The development of Hawaiian reefs may be influenced by
a combination of factors summarized by Davies and
Montaggioni �985! and Hopley �.983! such as initial karst
topography, sea level, island subsidence and carbonate
accretion. The reefs listed as types 1 and 2 in this study
are combined by Grigg �982! into his zone 1. Grigg �982!
described the processes characterizing this zone as
subaerial erosion, subsidence and fringing reef development.
The biogeomorphological progression of Hawaiian reefs
99
suggested by both Littler �985! and Grigg �982!, however,
are not evident on all reefs in the Hawaiian Archipelago.
For some unknown reason, reefs characterized as types 2 and
4 in the present study, lack large shallow areas such as the
RIDGE zone. Laysan has a small fringing reef. These reefs
are extremely small, in comparison to all other reefs in the
Hawaiian Archipelago. They have not apparently followed the
sequence of reef developmental events described by Littler
�985!. The absence of shallow reef area RIDGES! suggest
that they are not keeping pace with the destructive
processes described by Grigg �982!.
Standard Reef Performance:
The latitude at which reef growth cannot keep pace with
subsidence and physical and chemical destructive processes
has been termed the "Darwin Point" Grigg, 1982!. Grigg
�982! concluded, based on growth studies of the hermatypic
coral ~oites locate, that reef accretion decreaeed linearly
with increasing latitude from Hawaii to Kure Atoll Grigg,
1982!. Environmental factors, such as temperature and
light, may limit reef growth at high latitudes Grigg,
1982!.
Several investigators have shown, however, that
carbonate production does not vary with latitude see
Kinsey, 1985 for summary!. Carbonate production on high
latitude reefs, such as the Abrolhos Islands Smith, 1981a!
100
carbonate Figure 19!. The percent of carbonate
production attributable to coralline algae varies with
latitude and increases from less than 14 of the total
carbonate production on Hawaii and Maui to over 804 at the
most northerly sites Figure 19!. The increase in percent
coralline production is probably a result of several factors
including; an increase in area and percent living cover
inhabited by coralline algae and the high and, constant
II * * ~ KQllJIR
j!ILIUgl th 1
The effects of temperature, solar radiation and calcite
saturation state in controlled microcosm experiments on the
K t P
101
and French Frigate Shoals Atkinson and Grigg, 1984! was
comparable to measurements reported for reefs at more
tropical latitudes. Estimated carbonate production on
Hawaiian reefs between 23 and 28 North latitude Table
10! determined in the present. study closely approximates the
standard. reef performance for a reef ecosystem,
l.0 x 10 grams m y Figure 18!, calculated from Smith
�978!. The biogeomorphology of the Hawaiian reefs between
these latitudes, types 2,3,4,and 5 Table 7!, is variable
and does not appear to influence standard reef performance.
Standard reef performance in the Northwestern Hawaiian
{ 2 30 29o N . 1 atitude ! is apparently 1 arge 1 y
maintained by coralline algal production of calcium
TABLE 10. Carbonate production by coralline algae andcorals estimated hy zone on individual reefs
CARBONATE PRODUCTZON grams m y !
CORAL TOTALCORALLZNE ALGAE
BRANCHED CRUST
RZDGE RIDGE
CRUST
REEFREEF
42
5
5
928
102
KURE 18
NZDWAY 20
P&H 40
LZS 16
LAYSAN 14
NARO 192
GARDNER
FFS 320
NECXER
NZHOA
OAHU 60
MAUZ 4
HAWAZZ 4
38
42
210
84
74
126
210
23
23
147
272
406
195
315
284
420
420
515
34
34
13
13
85
170
350
420
50
420
252
585
1,2602,0502,880
93
98
482
542
844
933
365
1, 134672
1, 0051, 8772, 0932,922
FXGURE 18. Total estimated carbonate production hy coralsand coralline algae on some reefs in the HavaiianArchipelago. Dashed line represents a standard carbonate
production estimated from Smith �978!
103
0 4 N ao < 0
ev w � � O 0 0
L'" ~~<Oi jNOI13AClOHd 3l.b'NO8543 1VJ.Ol
104
FIGURE 19. Percent oi' total estimated carbonate productionby coralline algae throughout the Hawaiian Archipelago
105
o O 0 0 0 0 0CO CV
s } voisonaoza >co>v svi»vzoa3.06
species can adapt to environmental conditions at the
northern extremes of reef growth in the Hawaiian
Archipelago. This suggests that carbonate production by ~
1gl y1gl.
reefs throughout the Hawaiian Archipelago; a conclusion
substantiated by the geologic record on reefs in the
northern part of the Hawaiian Archipelago Gross et
al.,1969; Thorp �.936!.
The composition of calcareous organisms on Hawaiian
reefs considered in this study has been greatly simplified
and in essence represents a study in growth forms dominated
by coral heads and branched and crustose coralline algae.
Carbonate production by coralline algae is a primary factor
maintaining standard reef performance throughout the
Hawaiian Archipelago. This performance can be maintained
107
throughout a specific latitudinal range �3o � 28o N.
latitude! because of the physiological adaptability of
coralline algae and is not always dependent on
biogeomorphology. One factor which has not been considered
in this chapter is the importance of deep water carbonate
production by coralline algae in the Hawaiian Archipelago.
Estimated total annual deep water carbonate production by
coralline algae, bryozoans and H~a '~ed' may be equivalent to
total annual shallow water production Chapter XV!. Shallow
water reefs and deep water banks may be potential sources of
reactive carbonate particles dominated by aragonite, and
magnesian calcite compositions. In addition, shallow water
areas in temperate regions produce significant amounts of
magnesian calcite sediments. These particles may be of
importance to the dissolved inorganic carbon balance of the
Pacific Ocean Chapter XV!.
108
ZV. IMPORTANCE OF CORALLINE ALGAE IN THE OCEANIC BUDGETOF CARBON
INTRODUCTION
Smith �978! asked 4Do coral reefs constitute a
quantitatively significant ecosystem on a global scale' ?".
By considering the shallow water reef area between 0-30 m,
calcium mass balance, and fisheries yield of reefs, he
concluded that coral reefs should be included in
quantitative assessments of marine resources. This
assessment was confined to this depth range essentially
because of the availability of data obtained primarily using
SCUBA. The increased use of submersibles has provided
detailed descriptions of diverse and abundant tropical
marine communities at depths greater than 30 m. Deep water
banks �0-100 m! represent major sites of tropical and
subtropical fisheries in many island groups.
Deep water banks are found extensively throughout the
Hawaiian Archipelago Figure 17, Chapter III!. The depth
range of these banks defines an area composed of relatively
horizontal profile steep vertical cliffs are characteristic
of depths greater than 100 m! and abundant coralline and
other macroalgae Agegian and Abbott, 1985!. The lower
depth boundary of the deep water bank �00 m! is near the
base of the euphotic zone in this region; however,
macroalgae are found in relatively low abundance at deeper
depths receiving less than 14 surface radiation Agegian and
109
Abbe-.t, 1985; Littler et al.,1985!. 'major local fisheries
for slipper lobsters, spiny lobsters and some deep water
bottom fishes are located on these deep water banks Uchida
et al.,1981!.
The widespread distribution of coralline algal
communities on deep water banks has been verified by direct
visual observation using submersibles and from dredge hauls.
Coralline algae have been collected by various investigators
Adey et al., 1982; Dana, 1970! on deep water banks Figure
17! throughout the Hawaiian Archipelago. A rich assemblage
of carbonate organisms consisting of coralline algal
R~htual 11<"
and several unidentified species!, bryozoans, pen shells
Othl " I~ l.l b d
between 40«90 m on Penguin Bank, Hawaii from the
submersible, Nakali'i Agegian and, Abbott, 1985! . A similar
community composition was described at Kure Atoll Dana,
1971! and from collections made by the submersible in the
Northwestern Hawaiian Islands around French Frigate Shoals,
Necker Island, and Nihoa Island Hawaii Undersea Research
Laboratory data hank!.
This study asks "Is the annual biogenic carbonate
production on deep water banks �0-100 m! comparable to
shallow water �-20 m! carbonate production?". The
importance of benthic carbonate production of magnesian
110
calcite and aragonite is assessed in relation to the
oceanic carbonate system.
METHODS
Areal coverage of deep water banks �0-100 m! in the
Hawaiian Archipelago was determined from bathymetric
contours defined on U.S. Coast, and Geodetic Survey charts
from Hawaii to Kure Atoll. Areal coverage was determined by
tracing the bathymetric contours onto a transparent grid
sheet and counting the squares.
Areal coverage Table ll! and carbonate production
Table 12! in shallow water areas in the Hawaiian
Archipelago were determined as described in Chapter III.
Because of a lack ai data on several islands, the carbonate
production estimates for Kaula, Niihau and Kauai were based
on data obtained on Oahu, whereas Molakai, Lanai, and
Kahoolawe estimates were based on data obtained on Maui.
The percent cover of coralline and bryozoan communities
between 60 and 100 m was estimated on Penguin Bank, Hawaii,
from the submersible, Makali'i. Photographs of the
substratum were taken with 'a 35 mm camera mounted externally
on the submersible. The submersible cruised at a fixed
heading, speed and distance from the substratum. The
frequency of taking each photograph was determined by the
length of time required to charge the strobe approximately
30 seconds!; therefore, as soon as the strobe had recharged
another photograph was taken. Each slide was analysed by
projecting the slide onto a screen with 100 random points.
The percent of the area covered by sediments and living
calcareous organisms was determined by dividing the number
of points covered by the total number of points multiplied
by 100.
RESULTS
The deep water bank area between 20-100 m in the
Hawaiian Archipelago is approximately 1.6 x 10 m . The
DISCUSSION
The rate of deep water carbonate production is unknown.
Carbonate production rates characteristic of shallow watez.
112
average percent area covered by coralline algae and bryzoans
on two transects was 104.
Total shallow water reef area between 0-20 m in the
Hawaiian Archipelago is approximately 2.2 x 10 m Table
11!, The total area of the R1DGZ zone zepresents 154 of
the total shallow watez area between 0-20 m. The REEF area
represents 35% of the total shallow water area. The
remaining 504 of the shallow water reef area is dominated by
sediments'
Calculated total annual carbonate production on shallow
water reefs Table 13! between 0 and 20 m is 2.3 x 10
grams CaCO> y . Approximately one half of this production
is attributable to coralline algal production.
TABLE ll. Shallow water area between 0-20 m on reefs in theHawaiian Archipelago
SWALLOW WATER AREA
m !
RIDGE REEF
MIDWAY
P&H
LIS
LAYSAN
1.3O x 1O6GARDNER
9.02 x 10 1.13 x 10FFS
5.50 x lo
2 ' 20 x 10
MOLOKAI
LANAZ
KAHOOLAWE 3.20 x 10
1.80 x 10 1.44 x 10
5.90 x lo 4.72 x 10
MAUI
HAWAII
113
NECKER
NIHOA
KAULA
NIIHAU
KAUAI
4.63 x 10 5.65 x 10
7.71 x 10 9 43 x 10
7.48 x 10 9.36 x 10
5.57 x 10 6.96 x 10
2.80 x 10 1.84 x 10
7.52 x 10 9.40 x 10
1.95 x 10 2.73 x lo
4.77 x 10 6.68 x 10
8.35 x 10 1.17 x lO
7.11 x 10 9.95 x 10
1.30 x l0 1.04 x 10
6.00 x 10 4.80 x 10
TABLE 12. Estimated carbonate production hy corallinealgae and corals by morphology and zone on reefs in the
Hawaiian Archipelago
CQLRBONATE PRODUCTION
10 g CaCO3m y !
CORALCORALLINE ALGAE
BRANCHED CRUST
RIDGE
F 1 1 ~ 24 ' 22.0
1.22.1MIDWAY 2.0
FSH 2.0
4.2
5.910 ' 5
10. 5
10.5
10 ' 5
3.4
2.0 4.67 ' 4
LAY SAN 2 ~ 0
MARO 16. 0
GARDNER
7 ~ 68.8
14. 06.5
6 ' 3
16. 0 10 ' 5 7.4 16,8FFS
5.18 ' 4
8.4
8 ' 4 7.4
8.4 7 ~ 4
7.48 ' 4
8.4 7.4
1.85 ' 3
5.3 1.8
1 ' 8
5.34 ' 0 0.4
4.0 0.4HAWA 5 ' 3
1l4
NZCXER
NIHOA
KAULA 12.0
NXIHAU 12.0
KAUAI 12 ' 0
OAHU 12.0
NOLOKAI 4.0
LANAI 4. 0
KAHOO
11. 7
17.5
17.5
17.5
18.0
25 ' 6
25.6
25 ' 6
25.6
36. 0
subarctic to tropical coralline algae; however, provide a.
range of estimates. High growth rates �.6-2.7 cm y ! re
characteristic of branched tropical and subtropical species
Steneck and Adey,1976; Chapter X!. An intermediate growth
rate �.1-0.6 cm y 1! is typical for tropical and
subtropical crustose coralline algae Steneck and Adey, 1976
Comparatively slow growth;Agegian, Chapter III! .
115
�.04-0.2 cm y ! is characteristic of subarctic and some
temperate coralline algae Adey, 1970!.
The broad depth distribution of many coralline algal
species several species inhabit depths ranging from the
intertidal zone to 100 m, Adey et al., 19B2! and apparent
adaptability of these species to depth-related changes in
physical and chemical environmental conditions suggest that
shallow water potential production rates may be applicable
to coralline algae living on deep water banks. For example,
the net apparent photosynthetic rate of deep water crustose
coralline algae incubated at l4 of surface illumination was
comparable to shallow water coralline production Littler et
al., 1985!. Evidence supporting the potential for
significant carbonate production at depth is provided from
long-term microcosm experiments. At lower than ambient
temperature �9 C instead of 26 C} and solar radiation �4
of surface illumination! regimes, the growth of P.
w r
ambient conditions. Average temperature and light conditions
at 100 m at Penguin Bank, Hawaii �1 deg,10' N, 157 deg
60'W! are about 21 C and 14 of surface illumination Adey
2 hllllOI1 1 I f p ~
than 30 m and yet is capable of considerable growth at. light
and temperature regimes characteristic of these deeper
depths. Therefore, a reasonable estimate of potential
production by deep water coralline algae, considering their
growth form and size range predominantly free-living
branched and nodule forms and free living and attached
crusts!, is 654 of the potential production of encrusting
coralline algae determined by this study.
The widespread distribution of coralline algal maerl
species at depths greater than 20 m throughout the Hawaiian
Archipelago suggests that of the percent area covered by
coralline algae and bryozoans determined on Penguin Bank,
about 104, can be applied to the total deep water bank area
�.6 x 10 m !. Estimated carbonate production on deep
water banks with a carbonate production of 1.5 x 10 grams
CaCO> m y �54 of the shallow encrusting coralline
production rate! at 104 of the deep water bank area �.6 x
10 m ! would result in an annual production of 2.4 x 10
grams CaCO>, an amount, equivalent to shallow water
prod~ction Table 13!.
Estimated total carbonate production by coralline algae
and corals between 0-100 m �.8 x 10 m ! in the Hawaiian
116
TABLE 13. Estimated annual production of CaCO> withinRIDGE and REEF zones by coralline algae and 'orals. Annualcarbonate production on each reef in the HawaiianArchipelago was calculated as the product of shallow water
reef area and carbonate production from Tables ll and 12
ANNUAL PRODUCTION OF CaCO>
» gv !
CORALLINE ALGAE CORAL
BRANCHED CRUST CRUST
RIDGE RIDGE REEF
0.9
1 ' 5
15. 0
ll. 1
0.6
120. 0
144. 0
1.9
3.2
78.5
58.5
2.9
79.0
94 ' 7
0 ' 2
5.7
10.0
8 ' 5
0 ~ 1
<0.1
0.1
0.2
0 ' 24.0
7.0
6 ~ 0
0.1
<0 ~ 1
0.1
0.3
SUBTOTAL 3 19 337 1, 170495
CORALLINE ALGAL TOTAL
CORAL TOTAL
TOTAL RZZF PRODUCTION
1, 1511, 170
2,321
117
KURE
MIDW
PkH
LIS
LAY
MARO
GARD
FFS
NEC
NIHOA
KAULA
NIIHAU
KAUAI
OAHU
MOLO
LANAI
KAHOO
MAUI
HAWAII
1 ~ 2
2.0
55.0
51.5
16.2
61.1
0.8
83 ' 64.6
1.8
2.049.4
86.6
73 ' 6
1.9
0 ' 9
0 ' 6
0.6
1 ~ 9
0.7
1.1
31.8
32.0
14 ~ 0
132. 0
0.1
189. 0
2 ' 8
2.6
4.8
117.0
205.0
179. 0
26. 6
12.3
8.2
36.9
170.0
Archipelago is approximately 5.0 x 10 grams CaCO3 y or
7% of the total annual shallow water production on reefs in
the North Pacific Ocean Smith, 1978!. Two thirds of this
production can be attributed to coralline algae on shallow
water reefs and deep water banks. For comparison, the
average global carbonate production for the pelagic ocean,
27 grams CaCO> m y Broecker, 1974!, applied to the
total deep water and shallow water area would result in an
annual open ocean carbonate production of 4.9 x 10 grams
CaCO> y
Magnesian calcite production by coralline algae from
shallow water reefs and deep water banks throughout the
Hawaiian Archipelago may be of importance to the regional
carbonate budget of the open ocean waters forming a portion
of the Central North Pacific Gyre. Dissolution of benthic
carbonate production may account for a percentage of the
alkalinity maximium Fiadero, 1980; Better et al., 1984!
observed at intermediate depths in western North Pacific
waters.
Shallow water reefs and deep water banks are potential
sources of reactive carbonate particles dominated by
aragonite, and particularly, magnesian calcite compositions
Berner and Honjo, 1981!. In addition, shallow water areas
in temperate regions produce significant amounts of
magnesian calcite Smith, 1972!. These carbonate particles
may be of importance to the carbonate balance of the Pacific
118
Ocean. Indeed, it appears that the alkalinity maximum
observed at intermediate depths in western North Pacific
waters cannot be accounted for on a mass basis simply by
settling and dissolution of pelagic calcite Betzer et al.,
1984!. Approximately 0.035 grams CaCO> m d must be
dissolved in surface seawater to account for the excess
alkalinity.
Berner �977! concluded that a significant amount of
the CaCO> sedimenting to the sea f1oor was aragonite
produced by pteropods. Betzer et al. �984! suggest that
part of the excess alkalinity can be attributed to large
pteropods that until their work were not sampled adequately
with sediment traps. We suggest that horizontal transport of
highly reactive carbonate particles from shallow and. deep
water point sources within the Pacific Ocean and their
subsecpxent dissolution may also contribute in part to the
observed alkalinity excess. The potential importance of
this process can be assessed by a calculation comparing the
magnitude of benthic carbonate production to the carbonate
flux in the Pacific Ocean needed to account for excess
alkalinity. The value of deep and shallow water carbonate
production determined in this study of 2.7 x 10 g m y
applied to the tropical-subtropical reef area of the Pacific
Ocean between 0-100 m approximately 2.7 x 10 m Smith,
1978; Smith, 1972! yields a total production of magnesian
calcite and aragonite of 7.3 x 10 g y in tropical and
119
subtropical waters. The average temperate shallow water
carbonate production of i.O x 10 g m y Smith, 1972!
applied to the temperate shallow water area between 0-30 m
8.0 x 10 m ! Smith, 1978; Menard, 1966! results in an
annual temperate production of 3.2 x 10 g y . Therefore,
the estimated. total benthic carbonate production in the
Pacific Ocean is 10.5 x 10 g y , and if dispersed
throughout the entire Pacific Ocean area �80 x 10 m !
results in a potential carbonate flux of 0.016 g m d
obviously, only a portion of the total amount o f
benthic carbonate production may dissolve. Smith �972}
attributed the lack of carbonate sediment accumulation on
the temperate mainland shelf of southern California to
sediment dispersal and subsequent dissolution. Land �979!
calculated that approximately 50% of modern reef
productivity measured on the North Jamaican Island slope
dissolves in adjacent deep water. If this value were
applicable to the Pacific environment as well then as much
as 25% of the observed alkalinity excess of 0.035 grams m
day could be attributed to dissolution of aragonite and
magnesian calcite of benthic origin. Whatever the case, the
production, transport and magnitude of the subsequent
dissolution of benthic carbonate production need be
considered in the alkalinity balance of open ocean water.
120
V. CONCLUSIONS
Controlled microcosm experiments indicate that the
f ~ ~ l. i
influenced by growth rate. Physico-chemical factors of
seawater temperature and calcite saturation state influence
the magnesium content of this alga. The evidence supporting
this conclusion is three-fold.
Light experiments do not support the growth rate
hypothes's. Decreases in growth rate at low light levels are
not correlated with changes in magnesium content Figures 8,
11! as would be predicted by the growth rate hypothesis
proposed by either Moberly �968! or Kolesar �973! .
Temperature experiments do not support the growth rate
Experimental data describe a linearhypothesis.
121
relationship between magnesium content and temperature
whereas the relationship between growth rate and temperature
is curvelinear Figures 12, 9!. Growth rate decreases with
increasing temperature without a concomittant decrease in
magnesium content. Conversely, magnesium content decreases
with decreasing temperature with little change in growth
rate. Therefore, when the temperature regime in the natural
environment exceeds optimal conditions for growth, growth
rate is reduced without a reduction in magnesium content.
A physico-chemical control of magnesium content is
further suggested by the overall similarity in equations
describing the relationship between magnesium content and
temperature {Table 4!. Seven genera of coralline algae and,
three classes of benthic invertebrates are represented by
approximately identical relationships. This similarity is
remarkable, considering that the relationships were based on
1! a variety of methods used in the analyses of magnesium
content by various investigators, 2! coralline algae with a
wide range in external morphology, e.g. articulated and
crustose coralline algae, 3! coralline algae from different
oceans,and 4! coralline algal species characterized by
vastly different ranges in growth rates. The relationship
described by Chave {1954! ior calcareous algae is
dissimilar, perhaps because magnesium content was correlated
with average seawater temperature rather than collection
temperature. These relationships suggest that temperature,
and probably primarily calcite saturation state are
important environmental factors on a regional basis
influencing the magnesium content of coralline algae.
under controlled environmental conditions is influenced by
the calcite saturation state and temperature of seawater
Figures 12, 13!. These two variables account for S9% of
d l. y ~
controlled experimental environments, or a magnesium content
range of approximately 4.6 mole% HgC03 {Figure 15!. The
naturally occurring range in magnesium content of
~ d ' Y I.
122
between 0 and 28.5 N. Latitude was 6.3 mole 4 MgC03
Figure 3!. Therefore, approximately 734 of the total
natural range in magnesium content determined by this study
can be attributed to the effects of these two environmental
variables.
Systematic latitudinal variations in the magnesium
~ ~1~~ ~d ~~
study despite regional changes in environmental temperature.
I" "SS R-.
changes in regional temperature regimes Table 2! . Zt is
noteworthy that the algal 6 0 thermometer does not
resemble other carbonate paleothermometers; the algal 6 0
temperature coefficient is low in comparison with that of
other calcareous skeletons. Perhaps local variations in the
calcite saturation state of seawater Figure 14! owing to
biologic factors not temperature! effectively cancel the
regional temperature signal in terms of the resultant
magnesium content of the alga.
The environmental factors usually considered as
important in the growth of tropical calcareous organisms are
light and temperature. Historically, latitudinal limits of
coral growth have been defined by seawater temperature
Wells, 1957!. Grigg �982! reported a linear decrease in
the growth rate of one species of coral, Porites lobata with
increasing Latitude in the Hawaiian Archipelago between 19
and 29o N. Latitude. He attributed this decrease to changes
123
in both the light regime and, geawater 'mperature along a
latitudinal gradient. A similar scenario was hypothesized
g t tt g ~
laCCISrl decreases vith increasing latitude owing to
changes in environmental factors. ~ ~s' field growth
g ~ �. ~, g
systematic changes in growth rate with latitude Table 1!, a
conclusion which is consistent with the findings of Grigg
and Atkinson �985!.
Lower than ambient light and temperature regimes result
1 1 ' tt ~ g Bg!I1LCl
Figures 8, 9! . The ability of coralline algae to
species and decreased settlement of coralline crusts
Chapter 1I!. Diurnal changes in the calcite saturation
state of seawater in shallow marine environments Chapter
124
adapt to light and temperature regimes at the subtropical
limits of coral growth may in part explain the widespread
t g ~ ~
the Hawaiian Archipelago Chapter I!.
This investigation suggests that the calcite
saturation state of seawater influences the growth and
composition of biogenic magnesian calcites. Growth of
gtttgggt occurs in seawater undersaturated vith
g E. ~ g g ttt t t ~
Table 3!. Lover than ambient calcite saturation state
results in decreased growth and magnesium content in this
IX, Smith, 198lb; Kinsey, 1979; Smith and. Pesret, 1974;
Schmalz and Swanson, 1969; Broecker and Takahashi, 1966! may
be in part responsible for the local distribution of
coralline algae within biotic reefs.
Changes in environmental factors with latitude
apparently do not limit carbonate production in shallow reef
environments Gladefelter and Kinsey, 1985! on a community
level. The apparent paradox of this conclusion with that of
Grigg �982! can be resolved when the coral and coralline
algal components of a reef are considered in concert.
Carbonate production by coralline algae throughout the
Hawaiian Archipelago estimated from field measurements of
percent cover and growth rate was equivalent to or exceeded
carbonate production by corals on individual reefs
Chapter EII! at latitudes in which coral growth rate
becomes severely attenuated see Figure 7!. The transition
from a coral dominated community at low latitudes to an
algal dominated community at high latitudes without a change
in the metabolic rate of the community has been suggested by
Smith {1981!. Johannes et al. �983! suggested that
competitive relationships between macroalgae and corals on
reefs may establish latitudinal limits for the occurence of
coral reefs. Competitve interactions between corals,
bryozoans, and calcareous algae might explain the relative
abundance of coralline algae and bryozoans on deep water
banks �0-100 m! around the Hawaiian Archipelago where
125
hermatypic corals are rare. {Chapter IV; Agegian and Abbott,
1985! .
intertidal species but has been found at depths up to 30 m
Adey et al., 1982!. Light and temperature experiments
conducted in the present investigation Chapter II! suggest
h . ~ 1 p 1 hl g th
at light and temperature regimes characteristic at depths of
SO-100 m in the Hawaiian Archipelago. Dramatic visual
g 1 th ph hill. 1 t 1 h
occurred in the lowest light treatments within one week
after the iniation of the experiment Chapter 1Z! indicating
the ability of the alga to adapt quickly to low light
conditions. The broad depth distributions of many
126
tropical coralline algal genera Adey et al., 1982! further
suggests a broad light and temperature tolerance for this
group of algae. The ability to adapt to law light
conditions may in part explain recent findings by Littler et
al. �985! that the deepest plant life recorded, 268 m, or
0.00054 of surface illumination, is a coralline alga.
Current ideas on the light limitation of plant life in sea
must be reconsidered with particular attention to the
benthic macroalgae.
The most commonly predicted effects of an anthropogenic
doubling of atmospheric pC02 on the ocean in subtropical
regions are an increase in average surface seawater
temperature by 2-3 C and, a lowering average surface
seawater pH of approximately 0.5 units, hence, a lowering of
the calcite saturation state of seawater. The effects of
|' a a Lily
127
at only a few degrees higher than ambient temperature
Chapter lI!, a characteristic response for tropical marine
organisms living near their lethal limits. The growth of
corals and many tropical organisms is typically limited
within a narrow temperature range Jokiel and Coles, 1977!.
The experimental results indicate that the growth of
coralline algae may decrease approximately 60% in
association with a decrease in pH coupled with an increase
in temperature of surface seawater because of a doubling of
atmospheric C02.
Coralline algae may be important in the oceanic budget
of carbon, because they are potential sources of reactive
carbonate particles of magnesian calcite Chapter IV!, By
estimating �! the areal coverage of deep water banks and
shallow water reefs throughout the Hawaiian Archipelago, �!
the percent cover of shallow and deep water calcareous
communities and the carbonate production on shallow water
reefs from field experiments and the literature, and �!
the carbonate production on deep water banks from
extrapolations from experimental studies, the importance of
benthic carbonate production of magnesian calcite and,
aragonite was assessed in relation to the oceanic carbonate
system. The dissolution of a portion of the total benthic
carbonate production estimated for the North Pacific Ocean
could account for about 254 of the alkalinity excess noted
in western Pacific waters.
APPZNDIX I
Magnesium content analyses determined by atomic ahsorptionspectrophotmetry: raw data from microcosm experiments
129
Mole%
Nc}CO3
0.380.31
18.4618.60
2.762.20
I-A
18.53
0.300.23
17.3517. 49
2.38j.. 82
17, 4220,22j.9. 04
2.271.17
0.350.24
19.6318.5618.23
1.781.22
0,250.17
18. 391,661.10
0.240. 15
19.1218.35
18. 74
18.2618.31
2.142.39
0. 290.33
18.2919. 8720. 71
0.340.28
2.241.78
20.29j.. 481.25
19.1018.93
0.21G.ls
19.012.171.63
0.310.24
19.242.291.94
0,370. 3].
2j.. 09
19.06
130
Expel'amentHvmber ~ p ! Cagy !
19.0119.47
21.122i.06
Mean
~1
Grand Mean
18,37
18.14
18.45
17.12
17.55
18.17
17. 09
18.31
l7.94
18.29
Kxper imantNeer ~M ge!
0.310.54
0.180.30
0.320.28
0,090.19
0.100.08
0.290 ' 28
0.230.18
0. 410.30
0.170.32
0.150.36
~Ca m!
2.343.88
1.342.23
2.332.02
0. 761.48
0.780.62
2.122.09
1.841.41
3.022.20
1.302.40
1.102.62
Mole%
M9CD3
18.1518.60
18.0218.25
18. 4618,44
16.5817.66
17.5417,57
18.1918.14
17.0217.15
18.4218.21
17.8618.02
18.2018.38
Mean
~l S.D. N
0,32 2
0.16 2
0.02 2
0.76 2
0.02 2
0.04 2
0.09 2
0.14 2
0.11 2
0.13 2
Grand Mean
17.94
S.E. N
0.16 20
Mean
19, 27
19.50
20.53
19.14
19.07
18.55
18.62
18. 95
18.83
18.84
Exper imentNumber ~ ~!
0.150.38
0,270.43
0.320.46
0,300.26
0.370.23
0.360.25
0.340.28
0,210.33
0.270.21
0.210.37
Ca ~!
1.082.59
1.842,98
2.072.91
2.071.81
2.531.68
2.551.88
2.442,02
1.542.25
1.891.53
1,462.64
Mole%
19. 1019.44
19.6219,37
20.4220,63
19.1719.12
19. 4618 ~ 67
19.0018.10
18.7718.47
18.5319.38
18.8418.82
8.8318.84
0.23 2
0.18 2
0.14 2
0.04 2
0.55 2
0.64 2
0 ' 22 2
0.60 2
0 F 01 2
0.01 2
Grand Mean
19.13
S,ED N
0.18 20
S.D.
0.090.21
0. 721.61
17.55
0.310.25
2.502.].8
16. 53
0.140.20
1,071.66
17.12
2. 322.53
0.310.33
17.68
1.912.03
0.260.30
18.85
2.251.82
0.280.].8
15. 4917.3217,23
2.811.11
0.360.14
17.2718.2017.91
1.151.92
0.15
0.2518.06
17.1216.58
0.871.34
0.11
0.1616.85
18.5718.02
0.200.15
1.461.13
18,30
17.36
133
I~ ! C~a e!Mole%
17.7117.39
17.0516.01
17.5016.75
17.8117.55
18.3719.33
17.2313.75
Grand Mean
0.22 2
0.73 2
0.53 2
0.19 2
0,68 2
2.46 2
0.06 2
0.20 2
0.38 2
0.39 2
S.Z. M
0.30 20
0,220.31
1.492.05
I-L
19.85
0.250,38
1.622.46
20. 12
0. 220.34
19. 7218. 69
1.462.46
19. 20
2.232.76
0.330.
19. 69
2.092.12
0,320.33
20. 26
2.962.25
0.410.32
l8.93
19.1819.55
2.341.33
0.340.20
19.36
19.8619.75
1.451.69
0.220. 25
19.80
2.121.57
0.290.23
18.721.591.58
0. 230.3.7
17.34
19.33
134
Exper imentNumber ~w ~! C~a ~!
Mole%
19. 7919.92
20. 0120.23
19.6919.68
20.3420.17
18.6519.21
18.2219.21
19.3015.37
Sean
I NN
Grand Mean
0.09 2
0.16 2
0.73 2
0.01 2
0.12 2
0.40 2
0.26 2
0.08 2
0.70 2
2.78 2
S.E. N
0.27 20
0.260.25
15.9416.11
2.232.12
16.03
0.170.15
16.6415.96
1.421,29
16.30
0.250.25
2.092.18
16.27
2.231.74
0.250.20
16.03
0.260.20
2.121,73
16.47
1.772.24
0.210.26
16.24
3.121.19
0.360.13
15.82
0.843.01
0. 100.36
16 ' 42
3.123.48
0.370.41
16.2816.8016.52
0.140.27
1.142.22
16.66
16,25
135
~Ca ~!Mole%
MgC03
16.4716.06
15.7916.27
16.6316.32
16.3916.09
15.9315.71
16.4116.43
16.4116.15
Grand Mean
sole%
17.8118.11
0.250.26
1,881.96
EI-D
17. 9617.4317.79
0.360.43
2. 783.31
17.61
0.851.79
0.110.23
17.821.832,09
0.250 28
18. 0117,3217.27
0.390.41
3.033.27
17.2917.8618.15
2.493.45
0.330.46
18. 01
17.8717.64
0,150.14
1.131.07
17.76
16 ' 7516.90
1.861.67
0.230.21
16.8217.9517.31
0.280.35
2.092.72
17. 6317.9517 ..7
2.280.70
0.300.09
17.96
17.69
136
Exper imentNumber
18. 0617. 57
18 ~ 0817.94
Mean
~1
Grand Nean
~1
0.21 2
0.25 2
0.35 2
0.10 2
0.04 2
0.20 2
0.17 2
0.11 2
0 l5 2
0.01 2
S.E. N
0.12 20
Mole% Mean
~1Mgl~ ! ~Ca e!
0.380.59
19.4519.37
2.574,07
19.41 0.05 2
0.210.46
18.5619,74
1.523.07
0.83 219. 15
0.340,33
2.472.28
18.91 0.53 2
0.410.30
2.852.13
0.09 219.1219.3118,93
2.303.15
0. 330.45
0.26 219.1218.4917.84
2.070.93
0.290.j.2
0.46 218.1618.9718.97
2.512.51
0.360.36
0.00 218.97
19.2618,79
0.310.25
2.131.81
0.33 219.02
0.170.22
1.24
1,5618.50 0.38 2
1,931.93
0.280.28
0.00 219.15
Grand Mean
137
18.5419.29
19.1919.06
18.2318.77
19.1519.15
18. 95 0.11 20
0. 320,45
3.223.28
16.11
0,130,32
0.952.37
18.62
0.380.32
2. 762 ' 36
18.31
1.852.80
0.260.38
18.50
1.962 ' 09
0. 270.29
18. 63
0.450.32
5.552.36
15.].2
0.440.05
3.110.39
18.18
0. 090.29
0.642.26
18.04
0.941.03
0.1.30.14
18.45
0 ' 350.16
17.7517.53
2.641.28
17.64
17.76
138
M~ ~i! ~Ca ~!Mole%
13. 9118, 32
18.9518.28
18.3318.30
18.6018.40
18.6718.58
11.8018.44
18.8111.55
18.4817.59
18.3918.50
Mean
II
Grand Mean
3.12 2
0.47 2
0 ' 02 2
0.14 2
0.07 2
4.70 2
0.89 2
0.63 2
0.08 2
0.16 2
S.ED N
0 ' 38 20
MeanMole%
Mg003
15. 7415. 90
0.190.17
1. 651.47
15.82
15,4915.71
0.250,18
2. 241.58
15.60
16.3916.40
0.360.35
3.02
2.9316.39
16.2916,64
2.723.15
0.320.38
16.462.572.76
0.310.32
16.252.322.05
0.280. 24
16.60
15.7415.94
2.901.84
0.330. 21
15.84
2.282.51
0.320.28
15.632.011.31
0.240.61
16.582.452.69
0.320.34
17, 31.
16.25
l39
Nc~fgm! ~Ca m>!
16.4016.09
16.S216.38
15.6615. 60
16.3616.81
17.5617.05
Grand Mean
~l
0.11 2
0.15 2
0.01 2
0.25 2
0.22 2
0.31 2
0.14 2
0,04 2
0.32 2
0.36 2
S.E.
0.17 20
~M vm!
0.220.39
0. 130.13
0.360.26
0.300.21
0,250.35
0 ' 370.33
0. 330.19
0.310,28
0.210.24
14'2
~CR fill!
1.813.17
0.990.99
2. 762. 00
2.421.84
1.862.72
2.702.59
2.581.38
2.352.21
1.681.85
1.072.32
ale%
16.7317.01
18.1518.15
17.8117,76
16 ' 76%8
1, .88
17.36
18.5917.56
17. 4118.27
17.7917 ' 35
17.2617. 54
17. 4818. 45
Mean
Hole% NQ
16.87
18.15
17.79
16,27
17.62
18. 08
17.84
17.57
17. 40
17. 96
Grand Mean
~!
17.55
ale% MeanExperimntHerder Ni~f~! ~Ca cn!
0. 500. 29
III-D 3.862.28
0.14 217.42
0.270.29
1,872.03
0.14 219.36
0.390.25
19.9318.87
2.581.74
19.40 0.75 2
3.824.76
0.560.69
19.4119.20
19.30 0,15 2
19.7218.99
3.442.44
0.510.35
0.51 219.3620.2420.16
0.340.27
2.221.74
0.06 220.20
0.480.22
17.9218.32
3.661.64
0.29 218.1217.5517.72
0.95
1.060.12
0.1417.64 0.12 2
2.882.70
0.440.39
20.0319 ' 18
19.60 0.60 2
19.1219.38
0.803.31
0,110.48
19 ' 25 0.18 2
141
17.5217,33
19. 4619.26
Grand Mean
~1
18.96 0.29 20
Mole'
Me<03Aean
0,280.26
18. 6318. 00
2,001.98
18.31
0.240,27
19, 0818.03
1.662.02
18,56
0.480. 41
20. B720.02
2.982.68
20.4520,7219.76
0.210.36
1.332.43
20.24
19.6719.65
0.270.35
1.832.35
19. 66
19.2319.67
3. 073.05
0.440.45
19.45
0.390.35
20.2020.00
2.522.32
20.10
0.270.25
1.94l. 70
19. 30
1. 891.46
0,270.21
19.31
2.641.76
0.390.26
19.57
19.49
142
Expel immitNumber
IIX-E
~Ca pe!
18.9819.62
19.1019.52
19.6219.51
Grand Mean
0.44 2
0,75 2
0.60 2
0,68 2
0,01 2
0.31 2
0.15 2
0.45 2
0.29 2
0.08 2
S.E.
0,22 20
MeanNolel
0.280.3.8
19. 5820.55
1.871.16
20.07
19,5719.23
0.260,29
1. 792.01
19. 40
19.7519.28
0.21
0.301.432.05
19.52
19.9519.67
0.330.30
2.171.99
19.8118.3418.84
0.360.30
2.632.13
18.59
20 ' 5019.28
0.240.28
1.561.92
19.89
19.8519. 27
O. 170.22
1.161.54
19.5618.7119.43
0.190.20
1.351.40
19.072.241.33
0.350.21
20.52
1.691.32
0.260 ' 20
20.00
19.64
143
~ pn! Ca ~e!
20.5520.50
19.9820.30
Grand Mean
0 ' 68 2
0.24 2
0.33 2
0.20 2
0.36 2
0.86 2
0.41 2
0.50 2
0.04 2
0.03 2
S.E. N
0.17 20
Mole%
0.220.32
18. 8518. 86
1.542.28
18.86
17.5617.51
0. 290.31
2,282.42
17.54
0.330.43
19,0419.15
2.312.99
19.09
0. 270.36
1.822,51
19.32
0.310.47
2. 203. 55
18.37
0.250.36
1.902.61
18.38
0.211,36
18.8818.50
1.519.90
18.69
19.3719.52
1.461.04
0.210.15
19.44
19.7519.40
0.200.20
l. 33l. 39
19.58
l9.2520.86
2,471,39
0. 360.22
20.06
18.93
144
N~ ~!
19,5519.09
18.8317.92
18.1018.66
Mole% 5~
Grand Nean
S.D. N
0.01 2
0.04 2
0.08 2
0.32 2
0.64 2
0.40 2
0.27 2
0.11 2
0.24 2
1.14 2
S.E. N
0.23 20
Mole%
0,400.42
20.3419 ' 07
2.582.91
19.70
0.330.44
19.4419.47
2. 282,99
19.45
17,2716.86
0.290.37
2.253.05
17.07
18.9219.16
2.373.03
Q,3h0.44
19,0419,3419.32
2. 683.32
0,390.48
19.33
3 ' 341.68
0.470.23
18,62
3.283.01
0. 470.45
19. 35
0. 430.41
3.122.90
18.74
3.092.93
0.440. 39
18.55
2.582.91
0. 400. 42
19. 70
18.95
145
CB ~6L!
18.6918.56
18.9519.75
18.4619.02
19.0018.11
20,3419. 07
Mean
~1
Grand Mean
0.89 2
0.02 2
0.29 2
0.17 2
0.01 2
0.09 2
0.56 2
0.40 2
0.63 2
0.89 2
$.E. N
0.25 20
Hole%
N3C03
16.3416.55
0,150,22
1. 25l. 82
16,45
0.230.36
16. 5015,97
1.923.10
16.24
0,170.13
16.1416.89
l. 471.03
16.5215.9815.39
0.140.16
l. 241.41
15.6915.6715.10
1.181,65
0.130.18
15.39
0.260.17
2.221.47
16. 1616.37
16.26
0.200 ' 16
16.49l6,33
1.671.36
16.41
1.391.02
0.150.11
15.3215.33
l5.33
1. 792.65
0.230.33
17.42
2.492.30
0. 320. 29
17.28
16.30
l46
Kxper immitNumber
IIE-K
~M pn! ~Ca ~!
17. 6717. 17
17.5317.03
Grand Mean
S.D. N
0.15 2
0.37 2
0.53 2
0.42 2
0.40 2
0.15 2
0.11 2
0.01 2
0.35 2
0.36 2
S.E. N
0.22 20
Mole% Mean
18.10
18.08
17. 31
17. 45
16.37
17. 88
16. 90
17.75
17. 44
16.34
17,36
147
M~/ !
0.160.21
0.320.24
0.3.80,42
0.160.20
0,230.29
0.340.16
0.260.20
0.260.14
0,090,16
0.].10. 17
Ca ~ !
1.251.51
2.411.78
1.413.26
1. 221. 56
1.932.41
2,531.22
2,091.61
1.931.15
0.721.23
0.901.43
17,8018,40
18.1318, 04
17.0417.58
17.3617.53
16.2516,49
18.3017.47
16.7917.00
18.2717.22
17.4017.48
16. 34
16.35
Grand Mean
1ff0
0.42 2
0.06 2
0.38 2
0.12 2
0,17 2
0.59 2
0.14 2
0.74 2
0.05 2
0.01 2
S.E. N
0. 20 20
H~f~! ~ca ~! S.D.
XV-D
17,49 1.32
18.11 0.01
17.19
17.S4
18.90
17.81
16.77
l7,62
18. 02
17.37 O. 00
17. 68
148
ExperimentRmber
0. 220. 30
0.150.18
0.180.25
0.240.27
0.220.28
0. 260.35
0.290.29
0.210.26
0.250.30
0.170.17
1.822.17
1.101.37
1.432,03
1,962.03
1.611.87
2.012.55
2.282.41
1.641.97
1,942.17
l.31l.31
Wle&
NgCQ3
16.S518.42
18.1218.10
17.5916.79
17.0418.05
18.1119.70
17.35l8.26
17.1116. 43
17.4017.85
17 ~ 6218. 42
1"
1, 7
Grand Mean
0,57 2
0.72 2
1.12 2
0,64 2
0.48 2
0.32 2
0.57 2
S.Z. N
0.17 20
Mean
0,260.30
1,952.15
0. 27
0.160.15
1. 251.14
0.06
0.761.54
16.9518.47
0. 090.21
1. 07
19.5920.07
2. 03
1.730.300.26
0.34
2,392.09
18. 6718.86
0.330.29
0.1418.761.522.50
18.4820.54
0.210.39
1.46
19.78l7.93
1,891.57
0.280.21
18.85
2.182,30
19.7419.93
0.320.35
19,831.631,60
0. 250. 23
0.3419.65
1.821.85
0. 270. 29
20. 07
19.02
149
5~ ge!Mole%
NgC03
18.1918.57
17,5617.64
19.8919.41
19.8020.34
18. 38
17.60
17.71
19,83
19.51
1.31 2
0.13 2
0.38 2
0.28 20
V-A
16.91
17.71
18.22
17,32
18.55
18.21
18.01
18.51
17.76
18.97
18.01
151
Exper immitHUHlbCr
0,120.25
0.200.17
0. 210. 27
0.150.14
0.200.29
0.260.12
0.170 ' 17
0.150.13
0.180.19
0.260.21
~Ca ge!
0.972.03
1.551.34
1. 532.03
1.161.15
1.462.01
1.940.93
1. 271.33
1.100.93
1.331.45
1.781.52
Nole%
NgC03
16.7817.04
17.8817.55
18.2918.15
17.5717.07
18.1.218. 98
18.3218.10
18.3117,71
l8.4518.58
17.8317.70
19,2718.67
Grand Mean
~1
S.D,
0.19 2
0.23 2
0.10 2
0.35 2
0.61 2
0.16 2
0.42 2
0.09 2
0.09 2
0.42 2
S.E.
0.19 20
Mean
16. 0715.59
0.220.13
1.891.16
15,8315.7315.88
0.220.21
1.971.83
15.80
15.4716.14
0.180,37
1.593,14
15.81
0.210.39
1.853.34
16.001. 43l !3
0.170.16
16.620.290.23
2.551.96
16.05
0.090.12
15.50l5,59
0.841.08
15.5515.3614.73
0,650.63
0.070.07
15.0515.7915.56
1.101.53
0.120.17
15.67
2. 192,57
0.250.30
0.16,
Exper imentNmber b~f@~! ~Ca ~>
Mole%
15.8316.18
16.6816.56
15.9116.19
0.34 2
0.11 2
0.47 2
0.25 2
0.08 2
0.20 2
0.06 2
0.44 2
Q.'6 2
Grand Mean
15.84
S.E. N
0.13 20
Mole%Exper irrrentHurler
Mean
0.160.16
16.2720,08
1.401.05
VK
2,69 218.1716.4916.70
0.130.19
1.111.60
0.15 216.60
15.9815.72
0.150.14
1.311.26
0.18 215.85
l. 711.11
0.190.12
0.03 215.54
1.180.98
0.140.12
0,15 216.45
0.230.09
16,9916.00
l. 820.81
0.70 216.50
0.380.84
0.040.3.0
0.44 215.90
0.681.30
0.080.16
0.37 216.26
l6.6415.56
0,740.51
0. 090.06
0.77 216.1016,1716.03
1,502.63
0.180.30
0.10 216.10
Grand Mean
~1
153
~ ~! ~Ca ~!
15.5215.56
16.5516.34
15.5916.21
16.0016,52
16.35 0. 23 20
V-D
19.46
18.50
19.00
18.78
18.71
18. 14
18. 76
19.62
19.08
18.73
18,88
154
Exper identNumber ~ ~!
0,270.28
0. 220.25
0.310.30
0. 160.32
0.240,22
0. 230.21
0.200.21
0.120.25
0.270.22
0.420,24
Ca i~It~!i
1.861,90
1.641.78
2.172,16
1,162.21
1.671.63
1.791.55
1.431.51
0.851.63
1.851.61
2.841.79
Hole%
MgCG3
19.4819.43
18.3118.68
19. 1618. 83
18.4319.12
.15x4 ~ 27
17,7318.54
18,5818.94
19.2619.99
19.5718.59
19.4118.04
Grand Mean
S.D. N
0.03 2
0.26 2
0.23 2
0.4 2
0,63 2
0.57 2
0.25 2
0.51 2
0.69 2
0.97 2
S.E. N
0.14 20
Hole%
V-E
17.95
15,38
18.03
16.01
17 ' 18
16.48
15,85
17.31
16.24
17.11
16 ' 75
155
Exper identNunter ~ ~!
0.330.64
0.110.09
0.490.46
0. 120. 18
0.300.47
0.380.13
0.150.13
0.220.24
0.050,17
0.270.17
~Ca cn!
2.554.72
0. 960.80
3.633.46
1.081.53
2.473.68
2.971.16
1.31F 08
1,741.91
0.471.38
2.131,41
17.5618. 33
15.4715.28
18. 0718. 00
15.9216.09
16. 8217, 53
17. 2515. 70
15.6216.08
17.3117.31
15.5516.93
17.3116.90
Mean
~1
Grand Mean
~1
0.55 2
0.13 2
0.05 2
0,12 2
0.50 2
1.10 2
0.33 2
0.01 2
0.98 2
0.29 2
ST E. N
0.28 20
Hole%Exper identNumber McC<~! C~a e!
18. 6418. 50
0.190,15
1.361.06
18.57 0.10 2
18.0217.97
0.120.19
0.931.43
0,04 217.990.160.34
1,182.36
18.59 0.98 2
0.320.22
2.221.62
0,85 218.69
0.190.26
1.4l1.82
0.68 218.3418.7618.87
0.32O. 29
2. 272.02
0.08 218.82
14.0918.72
2.011.46
0. 200. 20
3.27 216. 4119.5119.01
l. 701.96
0.250.28
0.36 219.2617.9518.78
1.131.39
0,150,19
0.59 218,3718.7817.7S
1.491.86
0. 210. 24
0.71 218.28
Grand Mean
I NN0
156
17,8919.28
19.3018.09
17.8618.82
Ncaa
~1
18.33 0,24 20
Hole%
0.150.22
16. 6117.13
1.271.79
16.87
0,330.38
18.6117.99
2. 382.84
18.30
17. 7618.44
0.220.32
1,662.36
18. 100.160.23
l. 24l. 80
17, 191.781.89
0.240.25
17.99
18. 4118.20
1. 590. 95
0.220.13
18. 30
17.5717.73
l. 733.30
0. 220.43
17.65
2.282.93
0.310.42
18.4219.21
18.82
0.260.31
17.8417.79
1. 962. 39
17.81
17.89
157
Exper imntNumber ~ pn!
17. 2717,12
18.0117.96
1 NN
Grand Mean
1NN0
Mole%
18. 1518. 60
O.-L0,54
2.343,88
18,37
18. 0218. 25
0. 180.30
l,342.32
18.14
18.4618,44
0.320.28
2,332.02
18.4516.5817,66
O. 090.19
0. 761.48
17.1217.5417.57
0.780.62
0. 100. 08
17,55
18. 1918.14
0. 290.28
2.122.09
18. 17
1,841.41
0,230.18
17.093.022. 20
0,410.30
18.3117.8618.02
1.302.40
0.170.32
17,94
18.2018,38
1.102.62
0.150.
18. 29
17.94
158
Exper iment%mt r Ca ~l
17.0217.15
18.4218,21
Mean
~!
Grand Mean
0,32 2
0.16 2
0,02 2
0.76 2
0.02 2
0.04 2
0.09 2
0.14 2
0.11 2
0.13 2
S.E. N
0.16 20
19.40
17.66
17. 17
18.15
17.50
17.88
17.85
17.83
17,63
17.92
17.89
l59
Exper identNumber M~ pm!
0.410,34
0,190.14
0,210.17
0. 440. 20
0,260 ~ 14
0.290.24
0.260.30
Q. 270.23
0.070 ' 20
0.330.19
~Ca m!
2,762.40
1.461.10
1,631.37
3.151.56
1.941.09
2.201,81
1.922.34
2. 081. 79
0,561.50
2. 421.48
Mole%
MgC03
19. 7919. 01
17,9717.34
17.4516.90
18. 7817, 52
17.8317.18
18. 0617.69
18,3517.35
17,9017.76
17. 3917.87
18.5617.28
Mean
~1
Grand Mean
~1
Wlei Mean
17.52
17.81
17.30
17.82 p iq
17.91
17.98
18.07
17.03
17.46
18. 28
17.71
160
NcC ~!
0.230.26
0,260.28
0.130.16
0.271 9
.4
, il
0.190.31
0.200.38
0.230.23
0.110.31
0. 270,26
~ ~e!
1.802.01
2. 072.00
1.031.25
2.071.43
2.400.85
1.532,21
1.512.80
1.782.00
0. 882.30
1.981. 90
17. 4717,58
16 F 8818.74
17.0517, 56
l7. 747.89
18.8217.00
17.2518,72
17, 7418,39
17. 8216. 23
16.6518.28
18.2018.36
Grand Mean
0.07 2
1.31 2
0.36 2
l.29 2
1.04 2
0.46 2
1.12 2
l.l5 2
O. 11 2
S,E. N
0.12 20
Mean
0,170.22
20. 7120.36
V-L 1.101.44
20.53
1.412.22
0.220.35
1.032.47
0.150.37
2.001.38
0 790.20
19.25
20.9320,72
0. 522. 04
0,080.32
20. 7620.39
1.321.54
0,210.24
19.9819.74
1.511.52
0.230.23
19.86
1.141.85
0. 180 ' 28
1.631.74
0.240. 27
20. 251.202.13
0,190.31
Exper immitHUHltl8r N~ a>! Ca ~m!
Mole%
20.1620.58
18.9219.64
19.3519.15
20.6819,78
19.8120.69
20.9819,61
20.37
19.28
20.83
20.58
20. 23
20.30
0.25 2
0.30 2
0.51 2
0,14 2
0.15 2
0.26 2
0,17 2
P.63 2
0.62 2
0.97 2
Grand Mean
I MMl
20.14
S.E. N
0. 17 20
APPENDIX IZ
Magnesium content reported as grand mean mole 4 Mc' 0> andcorrected using reference standard.
162
CorrectedRef Grand Mam
~1Corr .
S,E,S.E.
18. 2718.1018.5316.8218.72
19.0617.9419.1317.3619.33
0.320.160.170.290.26
I-A
IC
IM
!-K
I-L
202020
20
20
22.4221.2722.2322,2322.23
0.33O.3.60. 180.300.27
16.2517.6918,9517,76
16.2517.6918.9517.76
20
2020
20
0,080.120. 110. 38
0.08
0.120.110.39
21.5021.502l.5021.50
ZZ-A
IZ-D
IZ-8
II&
17.6819.0217.49
0. 180.280.18
IV-D
IV-E
IV-F
17,6719.0117.48
21.5121.5121.51
0. 180. 280. 18
202020
163
Exper immitNumber
III-A
III-B
III-9
III-E
III-F
III'
III-H
III-K
IZI-L
V-A
V-B
VKV-D
V-E
V-F
VW
V-H
VM
V-K
V-L
Grand Mean
Nole 4
Ncg33
16. 2517.5518.9619.4919.6418. 9318. 9516. 3017, 36
18. 0115. 8416. 3518.8816.7518.3317.8917.9417. 8917. 7120.14
0. 170.190.290.220. 170.230.250.220.20
0.190.130.230.3.40. 280,240.200.160.160.120.17
21.5021.5022 ' 4222.4222.4221.5021.5022.4222.42
21.5021. 2721.2722.2321.5022.2321.2721.2721.5022.42
21.50
16.2517.5618.1918.7018.8518.9318.9515. 6416.66
18. Ol16.0116.5218.5416.7518.0018.0818.13
17.8916,9219.26
0.170.190. 27O. 200.160.230.250 ' 210.19
0.190.130.230.140.290.230.200.160.160.12
0.17
20
2020
20
2020
20
20
20
20
20
20
20
20
20
20
20
20
2020
APPZNDIX IXI
Summary of corrected mean gnesium contents and averagegrovth rates from a microcosm experiments
l64
State
~! S.E. S.E. N
1.621.30l.561.241.97
0.010.010.010.010,01
0. 320,160.170. 290.26
24.524.524.524.524,5
18. 2718. 1018. 5316. 8218. 72
500500
500250750
I-A
IMI-K
I-L
20
202020
20
10010
63
6363
303030
3030
19 ' 523.528.524.5
2020
2020
495
495500
496
0,080. 120. 110. 39
63
6363
63
1. 021.411.48l. 51
16. 2517 ~ 6918.9517.76
II-A
II-D
II-8
IIM
30
3030
30
0.010.010.020.02
0. 010.030 ' 04
404040
1.602. 001,39
17. 6719. 0117.48
6363
63
0,180.280.18
20
20
20
436772
235
27. 027. 027. 0
zxper identNurturer
III-A
III-8
III-D
III-E
III-F
IIIM
III-8
III-X
III-!
V-A
V-8
V<V-D
V-E
V-P
VWV-H
VMV-K
V-L
20.722.825. 025. 025. 030. 027. 425. 025. 0
27. 522. 0
22. 027. 527.527. 529. 0
29. 027.527.5
27. 5
449449450860590
455452
100255
413194411413
194
413415785
413254
785
63
6363
6363
63
6363
63
1006363
3063
7
63
63
636363
C.G.M,No3.e%
16.2517.5618.1918.7018.8518.9318.9515.64
16.66
18. 01
16. 0116. 5218. 5416, 7518. 0018, 0818. 1317.8916.9219.26
0.17.0.19
0.270.200.160.230 ~ 250. 210.19
0.190. 130,230.14
0,290.230.200.160.16
0.120.17
2020
2020
202020
2020
2020
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APPENDXX ZV
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BZBLZC APHY
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