LIMNOLOGY
July 1981
AND
Volume
OCEANOGRAPHY
Number
26
4
Limnol. Oceanogr., 26(4), 1981, 601-611
Estimating the daily contribution
of carbon from
zooxanthellae
to coral animal respiration1
L. Muscatine
Department
of Biology,
University
of California,
Los Angeles
90024
L. R. McCloskey
Department
of Biology,
Walla Walla College,
College
Place, Washington
99324
R. E. Marian
Department
of Biology,
University
of California,
Los Angeles
Abstract
An equation is derived which rigorously defines the photosynthesis
: respiration ratio (P:R)
for any alga : invertebrate
symbiotic association and permits the computation of the fractional
contribution
of translocated algal carbon to the daily respiratory
carbon requirement
of the
host animal. The equation is applied to two species of symbiotic reef corals, using 0, flux
data from 24-h continuous measurements
in situ. Given certain assumptions, the algae in the
shallow-water
Hawaiian reef corals Pocillopora
danzicornis and Fungia scutaria can supply
of the order of 63 and 69% of the daily respiratory carbon demand of their respective animal
hosts.
Symbiotic zooxanthellae
in reef corals
fix carbon dioxide by photosynthesis
and
translocate a substantial fraction of their
reduced organic carbon to the host coral
animal (Muscatine and Cernichiari
1969;
Lewis and Smith 1971; Muscatine
and
Porter 1977). Translocated
carbon is
thought to be of energetic significance to
the host since, in those corals studied, the
daily carbon input from feeding on zooplankton does not meet the coral animal
carbon requirements
for respiration
(Johannes et al. 1970; Johannes and Tepley
1974; Porter 1974). In addition,
some
symbiotic corals can live and grow under
l This work was supported in part by grants from
the National
Science Foundation
(PCM-33780
to
L.M. and GA-27941 to L.R.M.) and from Edwin
Pauley.
conditions in the laboratory where particulate organic carbon is excluded (Yonge
1930; Johannes 1974), implying that such
corals can satisfy all of their energy requirements from other sources including
translocation.
However, the quantitative
significance
of translocated
carbon has
not yet been determined
for any algaeinvertebrate
association.
As a point of departure, we asked the
question: how much of the daily carbon
requirement
for respiration of the animal
host is supplied
by the algae through
translocation?
Some investigators
have
tried to answer this question by using the
photosynthesis
: respiration
(P:R) ratios
of symbiotic corals. Typically,
daily P:R
ratios > 1.00 have been interpreted
to
mean that the coral is self-supporting
with respect to carbon. There are several
601
602
Muscatine
reasons why this interpretation
is basically untenable.
In many instances P:R
ratios are derived from short term measurements
extrapolated
to daily ratios
without appropriate justification.
In addition, the ratios are derived from oxygen
data but interpreted
as pertaining to carbon. Further, P and R arc rarely rigorously defined. Finally, and perhaps most
important, at least two additional parameters must be known before the magnitudc of algal contribution
can be inferred
from P:R. First the amount of fixed carbon translocated to the animal must be
evaluated. Only translocated carbon can
offset animal demands. Thus, a P:R of 2.0
for a symbiotic association may mean that
more C is fixed than respired, but, without translocation of the fixed carbon, the
animal is completely
dependent
on external sources and the system is not at all
phototrophic.
Second, we must know the
daily integrated value not only for total
coral respiration but also for the fraction
of this value due to animal respiration
alone. Only animal respiration can reflect
animal demands.
We derive here an equation which rigorously defines P:R for any algae-invertebrate association and permits the estimation of algal contribution
from p0,
measured continuously
in situ for 24 h.
We apply the equation explicitly
to measurements made on symbiotic reef corals
and estimate the contribution
of zooxanthellae carbon to host respiration in two
coral species. A preliminary
discussion of
how algal contribution
might be estimated has appeared elsewhere (Muscatine
and Porter 1977; McCloskey et al. 1978).
We thank R. Vance, C. Barnett, and R.
Highsmith
for critical reading of early
drafts of this manuscript,
many colleagues for discussions, the Hawaii Institute of Marine Biology for providing
facilities and support, and G. Ahearn for
the loan of space and equipment
at
HIMB.
Materials and methods
Or-ganisms-All
experiments were carried out at the Hawaii Institute of Marine
Biology, Kaneohe Bay, Oahu. Field ex-
et al.
periments were done on a shallow reef,
known locally as Checker Reef, 1.6 km
north of the laboratory. Two coral species
were studied:
Pocilloporn
damicornis
(Linnaeus), a branched colonial species,
and Fungia scuturia Lamarck, a solitary
unattached
form. Corals were selected
for size and condition and all macrocommensals (primarily
crabs and shrimp)
were removed from between branches of
P. damicornis.
Corals were handled only
under water and were used within 1530
min of collection.
Respirometry-Respiration
and photosynthesis of corals were measured in situ
at depths of l-3 m with two self-contained respirometers which continuously
record p0, in enclosed 45liter
Plexiglas
chambers containing
coral heads (McCloskey unpubl.). Each incubation lasted
for about 24 h, including
a l-min chamber flush each hour, thereby providing
data on total nighttime consumption
and
daytime consumption
and production
of
oxygen. After each 24-h incubation,
the
entire apparatus and corals were transported to the laboratory where coral displacement
volumes were measured so
that we could calculate absolute values
of oxygen in the incubation volume. Data
were normalized to mg 0, *liter-l *time-‘.
Estimuting
fructionnl
contribution
of
translocated
zooxanthellae
carbon to animal d&j
respiration:
Theoretical
and
practical
considerations-The
definitional equation below expresses the parameters of interest.
% of zoo2 gross C
Fractional
xanthellaecontribution
fixed
photosyn- * fixed C
of transtranslocatthe tically
located zooed to the
by zooxanxanthellae C
animal
the11ae
to animal
=
daily respiraC respired daily by ’
tory C
the animal
requirements
(1)
(CZAR)
Using the symbols and definitions
in Table I, we can abbreviate Eq. 1 as
CZAR
= v
a
(2)
Carbon jlux
Table
1.
Symbols
in symbiotic
and definitions.
Carbon :
R,
Carbon
respired
R,
Carbon
respired
by animal
R,
Carbon
respired
by intact coral
PZ
Gross carbon fixed photosynthetically
by zooxanthellae.
R,P indicate daily
totals; r,p indicate hourly rates (see
also F,f below)
Oxygen:
An “0” superior used in connection
with symbols above indicates terms
referable to oxygen
F”
tl,
t2
by zooxanthellae
Net oxygen flux by the coral. (All
respiration
values are considered to
have a positive sign. F” is typically
positive over a normal diel cycle.
However, fb may be negative at night
or positive during the day. See Fig.
1.)
Times of first and last detectable gross
zooxanthellae
photosynthesis
t(day)
Hours of daylight
24
Hours per day
between
quotient
we modify the theoretical equation to obtain a working equation so that all terms
can be estimated directly.
We derive the theoretical equation as
follows. Oxygen produced in photosynthesis and consumed by respiration
is
converted
to carbon equivalents
using
the photosynthetic
quotient (PQ) and the
respiratory quotient (RQ) where
mg C assimilated by zooxanthellae
photosynthesis
= mg 0, produced.0.375
PQ,-’
and
mg C lost by coral respiration
= mg 0, consumed.0.375
RQ,.
The gross carbon assimilated by photosynthesis
can thus be expressed
in
terms of 0, produced as
tl and t2
Other conventions:
T
A factor expressing percentage of
zooxanthellae-fixed
carbon which
translocated to the animal
PQ,
Photosynthetic
zooxanthellae
RQz
RQa
RQc
Respiratory
quotient
for zooxanthellae
Respiratory
quotient
for the animal
Respiratory
quotient
for intact coral
is
for
603
corals
P, = P,“.O.375 PQz-‘.
(3)
Since, by definition
the net oxygen flux
of the coral, F”, is the difference between
gross photosynthetic
oxygen produced
and oxygen respired by both the algae
and the animal, then
F” = P,” - R,” - R,”
(4
P,” = F” + &“.
(5)
and
Equation
3 can now be written
as
P, = (F” + &.“). 0.375 PQX-l.
where CZAR can be expressed as a fraction or as a percent.
Two problems arise in attempting
to
solve Eq. 2. First, because the factor T
applies to carbon translocated, all terms
in Eq. 2 must be expressed as carbon
quantities.
However,
the raw data for
photosynthesis
and respiration are units
of oxygen. This difference must be reconciled. Second, none of the terms can
be measured directly because of the obvious difficulties
of distinguishing,
in an
integrated 2-component
system, the values for the separate components. We approach the solution to these problems by
first deriving
a theoretical
equation
whose terms apply to oxygen data, and
second, with certain stated assumptions,
6)
Total daily carbon respired by the animal (R,) is obviously
some fraction of
that respired by the whole coral (h). Carbon respired by the whole coral is
R, = R, + R%.
(7)
If the ratio of carbon respired by the animal to carbon respired by the coral is
designated simply as p, then
R
p = e or R;, = PR,.
(84
and
1 - /3 = $
or R, = (1 - /3)h.. (811)
If these are converted
lents, then
to carbon equiva-
604
Muscutine
R, = /3(&O- 0.375 RQ,)
et al.
+24-
and
+18 -
R, = (1 - ,G)(R”. 0.375 RQ,).
(W
Computation
of photosynthetic
and respiratory quotients
is dealt with below.
Substituting
Eq. 6 and 9a in Eq. 2, we
h ave,
-f +12 ;:
cn
E +6-
(F” + &“). 0.375 PQz-l. T . (lo)
CZAR =
POC’ 0.375 RQJ
We can now obtain the working equation. At present, the experimentally
determined translocation
percentage (T) is
derived from short tenn experiments
utilizing 14C0, fixation in the light during
daytime (see below). From this methodology we must assume that translocation
occurs only during the daytime and that
factor T is independent
of light intensity.
Since algal carbon respired during the
day [designated
R,(day)]
will not be
available
for translocation,
it must be
subtracted from gross production, leaving
net production
[designated
P,net( day)].
Whereas net photosynthesis
is conventionally defined as
8
net = gross - respiration,
our modified
net(day)
expression
is
= gross - respiration(day).
10
12
2
‘!
4
6
= P, - R,(day).
(11)
From Eq. Yb,
10
12
2
4
6
-NNGHTTDAY----------cl
To facilitate the computation
of R,.” and
p, however, we must make two assumptions. Because daytirne respiration
cannot be measured during the period of
daytime irradiance
and photosynthesis,
we assume, as a first approximation,
that
the daytime rates of coral respiration are
the same as those measured at night. We
find the nighttime
rates to be virtually
constant. This assumption is depicted in
Fig. 1 by the straight lines extended into
the daytime period. Thus, R” can be
computed as
I
P,net(day)
‘2
8
Fig. 1. Representative
diel curve for a symbiotic
reef coral showing net 0, flux, 0, flux due to coral
respiration
(rCo), and 0, flux due to animal respiration alone (r,O). Vertical
arrows refer to rates of
oxygen production
and consumption.
Solid linc is
measured; broken lines are infcrrcd. Data from exp.
1 in Table 2.
R,” =
Thus,
~,(day)
I,,,,,,,,,,,,,,,,,,,,,,
24r2 dt = 24r,’
(15)
0
where r,O is the measured nighttime hourly rate of coral respiration.
Similarly,
p(day)
can be computed from
= (1 - ,@R<:“(day).0.375 RQ,. (12)
Equation
10 then becomes
{[(FO + R”). 0.375 PQ,-l] [(l - p)R”(day).0.375
RQJ}T
CZAR =
pK”- 0.375 RQ,
’
(13)
Figure 1 presents a plot of net 0, flux
(p) vs. time of day, derived from continuous p0, recordings. From such flux data
F”, the total daily net coral flux can be
obtained from
F” = CZ4P)dt.
RO(day) = 1’” rCodt = t(day)r,O.
11
(16)
Equation 16 will overestimate R,(day) in
Eq. 12 and underestimate
P,nct(day). As
long as (1 - p) is small, as it is for corals
in this study, these departures will be
slight. A precise, although less practical
expression for P,net(day) is given by
f/r
[(P + rCo)0.375 PQz-l
P,net( day) =
I 10
- (1 -P)
- I.(.”- 0.375 RQJ d t
Carbon flux in symbiotic
where ta and tb are the times just after
dawn and just before dusk when the algae are at their compensation point with
respect to carbon; i.e. when pz = r,.
Our second assumption is that respiration is proportional
to biomass, (B), as
measured by total protein, for both animal and algae. This allows calculation
of
the animal : coral (p) or algal : coral (1 p) carbon respiration ratio in terms of biomass ratio:
p+;
1-p+.
C
(17)
C
Substituting
Eq. 14-17 in 13, we obtain
our final working expression:
>
(W
or in a form more useful in computation
i2&3+ll
CZAR =
(1 -
P)~PQ:
RQ,)]
*T
P(RQc.
PQz)
UfW
where RQc is measured directly or estimated, along with PQ,, as described below. Note that in Eq. 18b the oxygen data
enter only as the ratio of net oxygen flux
(F”) to the oxygen respired by the coral
ho).
Photosynthetic
and respiratory
quotients-Equations
18a and b call for assignment of values for PQz and RQ,.
No universal value for PQz can be assumed to be applicable,
although this
quotient is often taken as 1.00. In the absence of direct measurements (considering that the chief nitrogen source for zooxanthellae
in coral cells is largely
ammonium
nitrogen:
Muscatine
and
D’Elia 1978), PQZ is taken as 1.10 (Raven
1976).
corals
6OFj
RQc can be estimated
directly
with
conventional
manometric
methods on
whole corals or indirectly by the formula
and assigning arbitrary values for RQZ
and RQa. As a first approximation
we
used the indirect approach, selecting values of 1.00 for the former and 0.8 for the
latter (cf. Kleiber 1961), although later we
show (Figs. 2, 3) the result of selecting a
wider range of values.
Algal : coral biomass ratios-To
make
an empirical determination
of representative algal : coral biomass ratios, we prepared tissue homogenates
by grinding
pieces of P. damicornis
or F. scutaria in
a mortar and pestle in 5 ml of “ZBS” buffer (Franker 1971) or by using a WaterPik. Homogenates
were further
processed with differential
centrifugation
followed by band velocity centrifugation
on a 3-step sucrose gradient. The clean
algal isolates were then assayed for algal
protein and chlorophyll
a. Once this ratio
was established
for zooxanthellae
from
each species of coral, we then extracted
and measured total chlorophyll
a and total coral protein for each experimental
coral head or specimen. Total algal protein was estimated from the formula
algal protein
*C Chl u = X algal protein
algal Chl CL
and expressed as a percent of the total
coral protein.
Translocation-We
estimated translocation of fixed carbon from zooxanthellae
to host tissues from rates of release of
fixed 14C by zooxanthellae
isolated from
P. damicornis.
The methods were those
described by Muscatine et al. (1972) with
the following
modifications.
Homogenates were obtained with a Water-Pik
and strained through several layers of
gauze. Isolated zooxanthellae
were suspended in half-strength
homogenate adjusted to 5-ml volumes. Each sample was
incubated at 27°C in a lo-ml graduated
test tube for 30 min with 5 PCi of
606
IMuscut ine et al a
NaIY4C03
at 250 pEinst*m-2
* s-l. Aliquots of final supernatant and resuspended algal pellet
were acidified
and
warmed to drive off unfixed 14C0, and
then assayed for radioactivity.
Analytical
methocls-Chlorophyll
a
was measured fluoromctrically
(HolmIIansen et al. 1965) in 100% acetone extracts of aliquots of tissue homogenate or
algal isolates deposited on glass-fiber filters (Whatman GF/C). Protein was mcasured by the method of Lowry et al.
(1951). Radioactivity
was measured by
liquid scintillation
counting and Aquasol
universal scintillator
(New England Nuclear).
Table 2. Release of fixed 14C by zooxanthcllac
isolated from P. damicornis.
Experiments
l-4 carried out under controlled light and temperature;
56 carried out under ambient temperature
and light
conditions.
Exp
‘I’ilne
Helcase of fixed ‘Y’,
(% of total fixed)
1
2
3
4.
5
6
0200
0800
1230
2000
1200
1230
27.2
51.1
46.1
38.9
45.7
39.6
periments. Table 3 shows that the carbon
fixed by P. dumicornis
and F. scutariu
zooxanthellae
and translocated to the animal tissue provides means of 63.2 and
Results
68.5% of the animal 24-h respiratory carBiomass rntios-Al
gal pro tein:chlorobon requirement.
phyll a ranged froin 16-36 for P. dumiTable 3 gives CZAR in tenns ofempircornis (n = 10) and 8-16 for F. scuturiu
ically derived biomass ratios and trans(n = 4). The calculated mean (-LSD) for location factor and arbitrary
values of
pcrccnt algal protein was 8.9 + 3.1 for P. PQm RQm and RQa; we also computed
durrLcornis and 3.2 IL 1.4 for F. scuturiu.
CZAR using a range of different values
2 gives the rc- for all of these parameters (Figs. 2, 3).
Trunslocution -Table
sults of six in vitro release experiments
Using the mean values of P,, r,, and
for zooxanthellae
from P. damicornis,
t (day) for P. chmicornis
and F. scu turiu
done at various times of day and night.
in Table 3, and given algal : coral respiThe mean of all observations
is 41.4%.
ration (biomass) ratios from 0.05 to 0.50,
This value is close to the 38 + 8.3% re- PQZ of 1.0 and 1.1, RQa of 0.7, 0.8, and
ported for release by zooxanthellae
iso- 0.9, RQZ of 1.00, the range of computed
lated from P. dumicornis
from the Great
values of RQ,, translocation at 30,40, and
Barrier Reef, Australia (Muscatinc
1967) 50% for P. dumicornis
and 15, 25, and
and 32.45% from previous in vivo studies
35% for F. scutariu, we can derive, by
(Muscatine
and Cernichiari
1969). As a plotting CZAR against algal : coral respifirst approximation
we chose 40% as the ration (biomass),
18 possible
curves.
translocation
factor in solving Eq. 18a, 1~. From the relative
positions
of these
For F. scutnrin we used 25%, as detercurves we see that percent algal contrimined experimentally
by Trench (1971).
bution is directly
proportional
to perRespirometry
and computation
of centage translocation,
but inversely proCZAR-A
typical diel curve for total oxyportional to RQ and PQz. Depending
on
gen flux by P. du*micornis is given in Fig.
the choice of parameter values above,
1. Such data, along with similar data for
CZAR can range from 41 to 136% for P.
IT. scuturiu,
yielded values for pXO, rVO, dumicornis
and from 36 to 180% for F.
and t(day) (Table 3). With RQZ set at 1.00, scuturia.
IiQ;, at 0.8, and algal : coral respiration
(biomass) at 0.09 for P. dumicornis
and Discussion
Measurements
of daily integrated oxy0.03 for F. scuturiu, we calculated values
species of
of RQ, from Eq. 19. Then, with PQ, set gen flux by two shallow-water
symbiotic corals, applied to our equation
at 1.1, P,net(clay) and R, were computed
(Eq. 18a,
as mg C. Finally, with translocation
fac- for estimating algal contribution
b), revcal that a quite substantial
fractors of 40 and 25%, we computed values
for CZAR in a number of replicate ex- tion of the daily respiratory carbon of P.
Carbon jlux
Table 3. Experimental
data and indirect
Calculations
based on percent translocation,
PQz = 1.10, RQz = 1.00, and RQa = 0.8.
(mpgZ&
(mg 21 h-l)
P. damicornis
in symbiotic
measurements
used to calculate
algal : coral respiration
(biomass)
P,net(day)
(mg C)
t(day)
03
(B,:B,
198
231
255
228
244
183
206
218
214
184
i = 215kSD
7.21
9.02
7.72
6.57
7.61
5.15
5.95
7.13
6.97
5.25
6.86
12.97
12.67
12.68
12.78
12.70
12.67
12.67
12.77
12.82
12.40
12.71
F. scutaria
(B,:B,
127
93
116
105
I! = 110.3+SD
2.43
1.87
1.60
2.00
1.98
12.00
11.93
11.72
12.30
11.99
corulu
P,net(day)‘T
(mg C)
607
CZAR from Eq. 18a, b.
ratios, and RQc as noted.
d$C)
CZAR
(%)
= 0.09, RQc = 0.815, T = 0.40)
64.9
75.6
84.2
75.4
80.5
60.6
68.2
71.8
70.5
60.9
72.4
26.0
30.2
33.7
30.2
32.2
24.2
27.3
28.7
28.7
24.4
28.5
48.1
60.2
51.5
43.8
50.8
34.4
39.7
47.6
46.5
35.0
45.8
54.0
50.3
65.4
68.8
63.4
70.5
68.7
60.4
60.6
69.6
63.226.9
17.1
13.1
11.2
14.1
13.9
63.0
Fj9.9
87.6
63.3
68.52 12.9
= 0.03, RQc = 0.805, T = 0.25)
dumicornis
and F. scutaria can be supplied from zooxanthellae.
Under the
local and seasonal conditions
of our experiments, the mean values are about 63
and 70%. The remainder of the animal’s
needs are presumably satisfied by intake
of particulate organic carbon (i.e. detritus
or prey organisms) or absorption of dissolved organic material or both.
Because of the assumptions involved
in calculating CZAR, these mean values
and their ecological implications
must be
regarded as tentative. Figures 2 and 3 are
intended to provide a guide to the possible dimensions of CZAR, given data or
assumptions other than those used here.
Thus if F. scutaria translocation percentage was 35%, with PQZ taken as 1.00,
then CZAR would be >lOO% and the coral would be viewed as phototrophic
with
respect to carbon.
Our assumption
that algal : coral respiration
is proportional
to algal : coral
biomass is based on the idea that respiration can be divided into growth respiration and maintenance respiration (Penning
de Vries
1975; Raven
1976).
According
to Raven (1976, p. 587),
“Growth
respiration
provides the ATP,
reductant and carbon skeletons required
43.0
31.5
39.4
35.3
37.4
10.8
7.9
9.8
8.9
9.4
for growth processes, and is directly proportional to the rate of growth. Maintenance respiration provides ATP for macromolecular
turnover
and for the
maintenance of solute gradients . . . ; it is
proportional
to biomass and not directly
related to growth rate.” Maintenance
also
includes “the processes of physiological
adaptation that maintain cells as active
units in a changing environment”
(Penning de Vries 1975, p. 77). The corals
used in our experiments
were large relative to their size range, and assumed to
be growing relatively slowly, if at all. The
respiration
detected in our 24-h incubation is therefore viewed as maintenance
respiration and as such is construed to be
proportional
to biomass. The empirically
derived algal : coral biomass ratios of 0.03
and 0.09 are similar to other recently
published biomass ratios for corals (0.14
for Pocilloporu
capitutu) and anemones
(0.08 and 0.09 for Anthopleura
eleguntissimu: McKinney
1978). Other indirect
approaches for estimating respiration ratios include the measurement of electron
transport activity (see Kenner and Ahmed
1975u,b) in isolated algae vs. coral animal
tissue and the measurement of dark respiration of intact corals vs. algae isolated
608
Vluscatine
et (11.
160
180
r
160
!OO
7
&
K
a
N
0
s
80
%
N
60
0
loo-
80-
60-
.A0
.20
.30
.40
50
1-B
Fig. 2. Graph showing how algal contribution
(CZAR) for P. damicornis
changes as a function of
translocation
(shape of symbol),
photosynthetic
quotient (upper or lower line in each set), animal
respiratory
quotient (number enclosed in symbol),
and (1 - p), the algal:coral
respiration
ratio (abscissa). RQ, (not included)
is fixed at 1.00, since
change in RQ, over normal range has an insignificant effect on algal contribution.
Some curves are
congruent or intersect. These are abbreviated
for
clarity of presentation.
from the same corals. These approaches
are only as reliable as the completeness
with which the algae and animal tissue
can be separated. For example, Downton
et al. (1976) gave a mean daytime dark
respiration
value of 28.15 pmol 0, *(mg
Chl a + c)-’ *h-l for zooxanthellae
isolated from P. dumicornis.
Converted
to
the same units, our value for r,O is 48.44
pmol. If 28.15 pmol is due to algal respiration alone then r,O is 20.29 ,umol andthe algal : coral respiration ratio would be
0.58, much higher than our estimate of
0.09 from biomass data. But as Downton
et al. pointed out, their dark respiration
rates were about 66% of the net photo-
01
0
'
Fig. 3.
I
.lO
'
I
.20
'
I
.30
'
'
.40
'
I
.50
1-B
Same as Fig. 2, for F. scutaria.
synthetic rate, and such unusually
high
respiration : photosynthesis
ratios could
be due to contamination
of the algal suspension by host animal cells. Since clean,
quantitative
separation of algae and animal tissue is virtually
impossible
for
many coral species, the use of aposymbiotic corals to estimate zooxanthellae
respiration rates from total respiration by
difference (i.e., R0 - R,” = R,“) emerges
as an important alternative method for future consideration.
The only drawbacks
of this method arc that measurements
must be normalized to some appropriate
parameter (such as biomass or surface
area) and will be limited to species for
which aposymbiotic
specimens can be
obtainecl. In addition, aposymbiotic
corals are not ideal controls since they lack
the translocated products normally used
as substrates for respiration.
Our assumption
that, for a given
Carbon flux in symbiotic
species and habitat, day and night algal
and animal respiration rates are constant,
should be considered only as a point of
departure until empirical
data become
available. The enigmatic question of the
rate of daytime respiration
of algae has
been reviewed by Raven (1976), who noted that it is still an assumption that the
respiration
of daytime illuminated
cells
is the same as that observed in an immediately
succeeding artificial dark period. Further, while it would seem that
the animal respiration component would
normally be unaffected by illumination
or darkness, both nighttime feeding (Porter 1974) and the periodic reception of
algal translocated products, as postulated
by Chalker (1977), may well cause respiration rates to fluctuate, as they do in
fed symbiotic
hydra (Pardy and White
1977). Mergner and Svoboda (1977) have
measured respiration
rates of a range of
symbiotic
cnidarians,
including
corals,
and describe
direct evidence
for increased oxygen consumption
in all associations in the initial hours of the dark
period compared to the remainder of the
nighttime
hours. A decrease in oxygen
consumption
with depth for a given
species, while not directly relevant to the
question of diel fluctuations,
has been
noted by Spencer-Davies
(1977) and
Mergner and Svoboda (1977). Obviously,
in specific cases where day and night respiration differ, the conventions
in Fig. 2
and Eq. 18a, b must be appropriately
modified.
Translocation
of fixed carbon from algal symbionts
to invertebrate
hosts is
now a firmly established
phenomenon,
supported by direct evidence from 14C
tracer studies (reviewed by Smith 1974)
and indirect observations of 13C:12C ratios
in algae and animal tissues of reef corals
(Land et al. 1975). F or each coral species
there still remains to be worked out the
fidelity with which in vitro release reflects in vivo translocation,
the daily integrated levels of translocation relative to
P,net(day), and the diel pattern of translocation. Although we can detect translocation at night in short term experiments that depend on artificial light, such
corxls
609
data must be interpreted
with caution.
No information
is yet available concerning translocation
during nighttime under
natural conditions.
An increment of net
carbon fixed during the day might be
translocated
later at night, and in that
case our formulation
would tend to underestimate the amount of carbon translocated. We assume that net carbon fixed
but not translocated is stored or used in
support of algal cell proliferation.
Although in the estimation of CZAR a
direct measurement of RQc is preferable,
we computed RQc indirectly as 0.815 and
0.805 using Eq. 19 and arbitrary values
of 1.00 for RQz and 0.8 for RQa. Our computed values of RQ, are somewhat lower
than values of RQ measured directly for
other intact symbiotic cnidarians such as
corals (0.86-0.90:
Kinsey
1978), sea
anemones (0.90-1.0: Pardy and Fitt unpubl.) and freshwater green hydra (0.86:
Pardy and White 1977). In view of the
high lipid content of reef corals (34% in
P. capitata),
and the metabolism
attendant to lipid storage and recovery, we
have used RQa = 0.8 so that the resultant
RQc might reflect at least a mixture of
protein, carbohydrate,
and lipid metabolism. Drew (1973) chose an RQ:, of 0.86
for several symbiotic corals based on the
assumption
that glycerol, a major substrate acquired by translocation, might be
immediately
metabolized by the animal.
From the foregoing discussion and the
rationale
for derivation
of the CZAR
equation, it should be evident that the
parameters P and R can be precisely defined, but have little relevance when defined in terms of oxygen data. For P:R to
be relevant to host reliance on algal production, the ratio must be expressed in
terms of carbon equivalents
and used in
conjunction
with translocation
data. By
using the expression
p.R = Pzn4dv)
Ra
’
we can compute from the data in Table
3 a mean P:R of 1.58 for P. damicornis
and 2.68 for F. scutaria. These ratios indicate only that the zooxanthellae
in P.
damicornis
and F. scutaria
produce
610
Musccltine
more carbon than the algae and animal
consume on a daily basis. The ratios by
themselves should not be taken to imply
any level of self-sufficiency
without data
on translocation.
Thus translocation
factors of 63 and 38% for P. damicornis
and
F. scutaria are required to achieve phototrophy with respect to carbon. Therefore, although our definition
of coral P:R
differs from other previous definitions,
the utility of ours, once translocation
is
established, is readily apparent.
On the other hand, P:R for isolated algae, either symbiotic
or free-living,
is
quite relevant to dependence on phototrophy since no translocation
is involved.
In such cases P:R can be defined prccisely with either oxygen or carbon values as
P,”
PZ
-RZ” Or R,
for isolated symbiotic algae (Table 4), or
simply Pnross:R for free-living
cells. Taking the data on oxygen-based
P:R, our
mean algal P:R values of 12.8 for P. damicornis and 47.3 for F. scutaria are much
higher than the values of 4.0 for cultured
free-living
Gymnodinium
(Humphrey
1975), I.5 for isolated P. dumicornis
zooxanthellae,
2.4 for isolated P. capitatu
(Burris 1977), and 5.15 for isolated Tridacna zooxanthellae
(Downton
et al.
1976). But since the latter values arc
based on short term rather than daily integrated data, such a comparison
may
have little relevance. The very high ratio
for F. scutnria may result from the relatively low values for R,24, which in turn
result from the selection of an algal : coral
biomass ratio of 0.03, and it may therefore
be subject to the same potential error as
the biomass estimation.
Since the ratio (P;T):R,
is an expression of a coral’s dependence
on phototrophic nutrition, such data are of considerable significance to studies on resource
partitioning.
Porter (1976) suggested that
algal contribution
will vary among coral
species, creating a spectrum ranging from
“phototrophic”
to “heterotrophic”
corals.
The equation
presented
here offers a
means of testing this hypothesis.
To a
et al.
Table 4. Experimental
data and calculated
ucs of algal P:R. Other parameters as in Table
val3.
Algal P:R
Displacemen1 vol
(ml)
Chl a
(4
222
111
159
165
205
108
160
165
202
128
R=
5.17
5.18
3.53
3.27
3.13
3.61
4.07
4.93
4.42
2.89
4.02
157
231
135
127
,f=
3.61
3.53
3.01
3.73
3.47
HA”
(w 0,)
-
P,” gross
P, gross
KU
H,
11.4
10.7
13.8
14.4
13.3
10.0
14.4
12.2
12.8
14.6
12.8
10.4
9.7
12.5
13.1
12.1
9.1
13.1
11.1
11.6
13.3
11.6
43.5
41.5
60.4
43.6
47.3
39.5
37.7
54.9
39.6
42.9
P. damicornis
17.3
21.6
18.5
15.8
18.3
18.3
14.3
17.1
16.7
12.6
17.1
F. scu taria
2.92
2.24
1.92
2.41
2.37
certain extent this has already been possible. For example, the daily integrated
0, flux for Pocillopora meandrinu as presented by Franzisket (1969a,b) and analyzed according to our equation (Muscatine and Porter 1977) suggests an algal
contribution
of 86.8%. Similarly, Wethcy
and Porter (1976), applying the principles described here to daily in situ measurements of PO, in Pnvona praetorta,
conclude that this species is capable of a
phototrophic
existence down to 25 m.
Both corals are foliaceous and have high
surface : volume
ratios and relatively
small polyp diameters, putting them in
the group designated by Porter (1976) as
specialized for light capture and, hence,
phototrophy.
References
BUHRIS, J. E. 1977. Photosynthesis,
photorcspiration, and dark respiration
in eight species of
algae. Mar. Biol. 39: 371379.
CHALKER, B. E. 1977. Daily variation in the calcification
capacity
of Acropora
ceruicornis.
Proc. 3rd Int. Coral Reef Symp. 2: 417-423.
I)owNToN,W.J.
S., D. G. BISHOP, A. W. LARKUM,
AND C. B. OSMOND. 1976. Oxygen inhibition
of photosynthetic
oxygen evolution
in marine
plants. Aust. J. Plant Physiol. 3: 73-79.
DREW, E. A. 1973. The biology and physiology
of
alga-invertebrate
symbioses. 3. In situ measurements of photosynthesis
and calcification
iii some hermatypic
corals. J. Exp. Alar. Biol.
Ecol. 13: 165-179.
FRANKER, C. K. 1971. Electrophoretic
identity of
polypeptides
from the nuclear membrane
of
Atrthopleurcl-associated
zooxanthellae.
J. Phycol. 7: 20-25.
FRASZISKET, L. 1969u. Riffkorallen
konnen autotroph leben. Naturwissenschaften
3: 144.
-.
1969b. The ratio of photosynthesis
to respiration of reef building corals during a 24 hour
period. Forma Functio 1: 153-158.
HOLM-HANSEX,
O., C. J. LORENZEN,
R. W.
HOLMES, AND J. D. STRICKLAND. 1965. Fluorometric determination
of chlorophyll.
J. Cons.
Cons. Int. Explor. Mer 30: 3-15.
HUMPHHEY, G. F. 1975. The photosynthesis:respiration ratio of some unicellular
marine algae.
J. Exp. Mar. Biol. Ecol. 18: 111-119.
JOHANNES, R. E. 1974. Sources of nutritional
energy for reef corals. Proc. 2nd Int. Coral Reef
s> lnp.
1: 133-137.
-,
S. L. COLES, AND N. T. KUENZEL. 1970.
The role of zooplankton in the nutrition of some
scleractiniaii
corals. Limnol.
Oceanogr.
15:
579-586.
---,
AND L. TEPLEY. 1974. Examination
of feeding of the reef coral Porites Zobatn in situ using
titne lapse photography.
Proc. 2nd Int. Coral
Reef Symp. 1: 127-131.
KEVSEH, R. A., AND S. I. AHMED. 1975u. Measurenients of electron transport activities in marine
phi\
toplankton.
Mar. Biol. 33: 119-127.
-,
AND p.
1975b. Correlation
between
ox! gen utilization
and electron transport activity iri marine phytoplankton.
Mar. Biol. 33:
129-133.
KINSE~,, D. W. 1978. Productivity
and calcification
estimates using slack-water
periods and field
enclosures.
Monogr. Oceanogr. flethodol.
5:
439468.
KLEIBER, M. 1961. The fire of life. Wiley.
LAND, L. S., J. C. LANG, AND B. N. SMITH. 1975.
Preliminary
observations
on the carbon isotopic composition of some reef coral tissues and
symbiotic
zooxanthellae.
Limnol.
Oceanogr.
20: 283-287.
LEWIS, II. H., AND D. C. SMITH. 1971. The autotrophic nutrition
of symbiotic
marine coelenterates with special reference
to hermatypic
corals. 1. 1Iovement of photosynthetic
products
between the symbionts.
Proc. R. Sot. Land.
Ser. B 178: 111-129.
LOWRY,~. H.,N.J. ROSEBROUGH, A.L. FARR,AND
R. J. RANDALL. 1951. Protein measurement
with the Folin phenol reagent. J. Biol. Chem.
193: 265-275.
~ICCLOSKEY, L. R., D. S. WETHEY, AND J. W. PORTER. 1978. The measurements
and interpretation of photosynthesis
and respiration in reef
corals. ;Llonogr. Oceanogr. Methodol.
5: 379396.
IICKINNEy,
I>. \I. 1Y'iX. ‘I’h e pt’rc’caiit contril)iitiolr
of carboil from zoox,uithellac
to the nutritioii
of
the \ea allenlone
A~~tho~~lr~rtr-c~clegallti.,sirl,tr
(Coeleiiterata:
Aiithozoa).
1I.S. thesis, \I’all,i
Walla College, College Placcl, i$‘,rsh. 45 p.
IIERGSER, H., AND A. SL OHODA. 1977. Protluctivit) alrd seasonal ch,tirgc\ in \tblected reef ‘rrc’a\
in the Gulf of Aqal)a (Reel Sea). Helgol. \ciis$.
\leeresuiiters.
30: 383-399.
\~USCA’I‘INE,
L. 196i7. <: 1.v cerol ei\cretion
bv 41 IIIbiotic algae fkom c.oral\ aiitl f’ritlacflcl
a11tl if4
control by the host. Science 156: 516-519.
---,
ASD E. CEIWICHMFU.
1969. Assimilatic,il
of‘
photos! nthetic proclucts of /oox~mthellae
I,! ‘1
reef coral. Biol. Bull. 137: 5Oh-523.
~~11 C. D’ELIA.
1978. ‘l‘hc llptak,
I-retI-2
tion aid release of amniotiiiiiii
l)! reef’ c~)riil~.
Limnol. Oceanogr. 23: 725-7:34.
-,
R. R. PO<& A\,11 E. (:KK\lCHIAKI.
1972.
Sonie factors influeilciiig
\elcctive
relea4cx of
soluble organic iriaterial by zooxanthellae
fi-olti
reef corals. Mar. Biol. 13: 29X-‘308.
AND J. W. PORTER. 1977. Keef coral\: \111->
tualistic symbiosis adaptetl to iiutrient-poor
~IIvironments.
BioScience 27: 454459.
PARDY, R. L., AND B. N. WHIIE.
1977. ;\letal)olic
relatioliships
between green hy,tlra and it\ x! IIIbiotic algae. Biol. Bull. 153: 228-236.
PENNING DE VRIES, F. 1975. I’lw cost of iiiaiirtc~naiice processe\ ill plalrt c*clls. AIIII. Hot. 39:
77-w.
PORTER, J. \V. 1974. Zooplairktoil
feedirrg I)\ thra
Caribbean reef-builtliiig
cor,il \lortfu,~f 02~ (‘(II ertlosu. Proc. 211tl Itrt Cola1 Ht~c~f‘Sy~lnp. 1 : 1 1 I 1.25.
-.
1976. Autotropll!,
hc~tc~rotrophy ,ltrtl rt’source partitioiiing
III Caril)l)t~an reef-l)riiltliilg
corals. Am. Nat. 110: 731-7-E.
RAVEN, J. A. 1976. ‘1’1~~~clualititatrv~e role of’ ‘tlark’
respiratory processes in heterotrophic
atlcl photolithotrophic
plairt grovvth. AIIII. Bot. 40: 587602.
SMITH, D. C. 1974. Transport f’rottr symbiotic, algae
and s! inbiotic chloroplast4 to host cells. Sv 1111).
Sot. Exp. Biol. 28: 485--,5?0.
SPESCER-IIAVIES, P. 1977. Carbon budget\
al~tl
vertical zonatioli of Athnitic reef corals. Proc.
3rd Int. Reef Coral S! mp. 1: 392396.
TKENCH, R. K. 1971. The phy siologv and biochetiiistry, of zooxanthellae
sy ttil)iotic with mariiic
coeleiiterates.
2. Lil)t~ratiori of‘ fixed ‘I<: bv LOOxanthellae in vitro. Proc. R. Sot. Loncl. Sclr. B
177: 237-250.
WETHE~, 1~. S., ANII J. W. Po~ux:I~. 1976. IIal)itatrelatecl patteriis of productiv,ity,
of the foliaceous reef coral, Puzor~cl practortu Dmra, p. TiCI65. III G. 0. Xlackie [ (~1.1, (1oeleiiterate
r~~)log!
and behavior. Plcnu111.
YONGE, C. 14. 1930. Stiltlies OII the phy siologv of
corals. 1. Feecliilg inechailisltr\
and foocl. S~SI.
Rep. Great Barrier Heef E\pt)tl. 1: I4-Fi7.
Sub~~rittccl: 10 April
Acceptd:
10 l>cwmlwr
1980
1980