The biology and physiology of alga-invertebrate symbioses. III. In situ measurements of photosynthesis and calcification in some hermatypic corals

J. rsp.

MW. Biol. Ecol.,

1973, Vol. 13, pp. 165-179;

THE BIOLOGY AND PHYSIOLOGY 111. IN SITU

C North-Holland

Publishing

OF ALGA-INVERTEBRATE

Company

SYMBIOSES.

MEASUREMENTS OF PHOTOSYNTHESIS AND CALCIFICATION IN SOME HERMATYPIC CORALS EDWARD

A. DREW

Gatty Mnrine Laboratory,

St. Andrew,

Scotland

Abstract: In sifu measurements of the rates of photosynthesis and calcification in three species ot hermatypic corals were made at Eilat, in the Gulf of Aqaba, Red Sea. Experiments were made at 5, 20 and 35 m depth under unusually poor conditions of submarine illumination for the region, and at the relatively low water temperature (21 “C) for coral growth which prevails there all year. Estimates of photosynthetic rates by both the ‘T and oxygen methods indicated that the ‘T method does measure gross photosynthesis in these organisms even at, and below, light compensation points. Substantial rates of carbon fixation in Acropora and Millepora show that, even under bad conditions, these organisms could survive autotrophically to at least 10 m depth, as also could the massive coral Goniastrea although this had much lower photosynthetic rates under the same conditions, compensated for by a much lower respiratory rate than the other two corals. Calcification rates were variable but showed a considerable increase in light as compared uith the dark in all three species, and the rates did not decrease with depth as much as might have been anticipated from the reduction in photosynthesis and ambient light energy. Photosynthetic and calcification rates were similar to those reported for similar organisms both in the Caribbean and on the Great Barrier Reef.

INTRODUCTION

Hermatypic corals are characterized carbonate skeletons relatively rapidly

by their ability to deposit substantial and so produce extensive carbonate

calcium reefs in

the tropical seas to which they are confined. Stoddart (1969) has reviewed measurements of coral and reef growth rates, and estimates are of the order of 1 cm increase in reef elevation per year; some corals such as Acropora show much higher growth rates whilst others such as the massive hemispherical ‘brain’ corals grow much more slowly. The work of Goreau over the last two decades, using the radioisotopes ‘“Ca and 14C to measure growth rates over short periods and of sp-cific parts of coral colonies both in the laboratory and it1 situ on the reefs of Jamaica, has produced much valuable information on both the rate and the mechanism of calcium deposition. His work is reviewed by Yonge (1963, 1968) and by Stoddart (1969). One of Goreau’s most important findings was that the rate of calcification is dependent on illumination, thus clearly implicating the symbiotic dinoflagellate zooxanthellac of all these hermatypic corals in the mechanism of calcification. The contribution of these symbiotic algae to the metabolism of such corals was studied by Yonge and co-workers on the Great Barrier Reef and they concluded that, under the conditions of their experiments, they were important in removing 165

EDWARD

166

waste products sulphur,

such as carbon

and enhancing

animal

dioxide,

A. DREW

nitrogenous

metabolism

compounds,

phosphorus

in this way (Yonge,

1931); however,

Yonge, Yonge & Nicholls (1932) found that the photosynthetic activity did not produce enough oxygen to compensate for animal respiration period and they did not consider the algae as potential animals, especially as the animal was found to lack suitable of the zooxanthellae

(Yonge,

and

suppliers enzymes

of the algae over a 24-h

of food to the for the digestion

1930).

More recently, Muscatine (1967) and Muscatine & Cernichiari (1970) have shown that the intact zooxanthellae are capable of supplying considerable amounts of photosynthetically produced material to the animal tissues, and Lewis & Smith (1971) have demonstrated the transfer of such material in the form of simple carbohydrates and amino acids within the intact association. The importance of the photosynthetic activity of the algae in hermatypic corals must therefore be considerable and some indication of how this varies with different conditions of shade and depth on the reef is important. In this paper, 45Ca, 14C, and oxygen methods, used by other workers on sh.allow reefs, have been extended to in situ studies of photosynthesis and calcification of hermatypic corals down to 35 m. The methods used were similar to those of Drew & Larkum (1967) and Drew (1969, 1973); they were originally developed from those of Goreau & Goreau (1959) and allow changes in metabolic rates with increased depth to be determined without the necessity for bringing the material to the surface with resulting damage from excessive handling, temporary emersion, and intense insolation.

MATERIALS

LOCATION

AND

AND

METHODS

CONDITIONS

The work was carried the Red Sea, latitude

out at Eilat, 29” 31’N, where

in the Gulf of Aqaba water

temperature

at the northeast

end of

is low for coral growth

(21 “C) and where reefs only develop because this temperature is maintained throughout the year. Conditions of submarine illumination during the experiments were particularly poor for coral reef regions because of recent heavy rain carrying suspended matter corals temporarily CORALS

into the sea: the results obtained, under adverse conditions.

therefore,

apply

primarily

to

INVESTIGATED

Experiments were carried out on three hermatypic corals - an Acropora species forming table-like colonies at 20 m depth, Milfepora tenera Boschma growing abundantly at 3 m depth, and a species of Goniustreu forming small ovoid colonies about 10 cm diameter on rock surfaces at 3 m depth. Approximately 7 cm long branch tips of Acroporu and Milleporu were used, and whole colonies of Goniustreu.

PHOTOSYNTHESIS

AND

CALCIFICATION

167

IN CORALS

The animals were not removed from the water at any time during periments until immediately before they were killed and preserved.

any of the ex-

In Sirlr INCUBATIONS Wooden

platforms

with spring clips to hold 6 experimental

jars were tied horizon-

tally onto the tops of coral heads at depths of 5, 20 and 35 m below low water mark on a sparsely colonized reef sloping at about 40” from the horizontal. This was 150 m south of the Eilat Marine Biological Station of Jerusalem University. A transect line marked at 10 m intervals was laid between the platforms for ease of re-location especially of the deepest site. All underwater work was carried out by standard SCUBA diving. At the start of an experiment, pieces of coral were broken off the colonies or substratum, and placed in Kilner preserving jars of 475 ml capacity and then transported to the different experimental platforms where the radio-isotopes were injected with hypodermic syringes through rubber ports set in special Perspex lids. The isotope solutions contained either only 45Ca (as CaCI,) at a concentration of IO &i/ml. or both 45Ca and 14C (as sodium bicarbonate), both at that concentration. I ml of the solution was injected into each jar resulting in isotope concentrations of z 20 /iCi in the incubation media; specific activities in the different experiments are TABLE

I

Specific radioactivity within incubation jars resulting from underwater injection of radioisotopes with repeating syringe, and relevant characteristics of the sea water: *because 45Ca has a relatively short half-life (165 days), incubation water and skeleton fractions counted at same time: no corrections, therefore, necessary for isotopic decay. Experiment

Species

Specific

radioactivity

45ca* _____ 2

4 5 Sea water characteristics:

temperature salinity inorganic carbon calcium content

‘YI ~~

8.3 9.9 7.2

Acropora Millepora Coniastrea .-

(cpm/lrg)

126 169 141 .____ 21 ‘C

content

42 eioO 32 /Lg/rnl 495 /(g/ml

given in Table 1. An experiment in which dye solution was injected under similar conditions indicated that the force of injection through a fine hypodermic needle ensured adequate mixing within the experimental jars. Dark controls were immediately wrapped in two layers of aluminium foil, all the jars then inverted and clipped onto the platforms where they were left for = 4-h periods starting at about noon in all cases. Dead animal controls were set up by treating pieces of coral inside small polythene bags with 50 ml of 40 % formaldehyde solution injected in immediately

EDWARD

168

before sealing

with rubber

bands;

after

A. DREW

IO min this treatment

caused

sation of 14C fixation in subsequent incubations in the light. During the experiments, ambient sea temperature was constant 21 “C. Ambient light intensity the estimation of the distance

complete

ces-

at all depths

at

at the start and finish of experiments was assessed by at which a black body (in this case the co-diver in wet

suit) could just be seen. These distances

(d), and the diffuse attenuation

coefficients

(K) calculated from them according to the formula, K = 1.5/d, are set out in Table II together with approximate values for the percentages of surface light reaching the experimental platforms. Underwater illumination corresponded to Coastal Types 1-3 of Jerlov (1951) and on one occasion deteriorated to Type 7 during the course of an experiment. True light intensities at the platforms were probably 2 20 on greater than calculated because of reflection from the light-coloured substratum. TABLE

Underwater

II

illumination estimated from ‘black-body’ visibility tenuation coefficients (K): water type according

data (d) and calculated to Jerlov (1951).

diffuse

at-

Experiment 2 d

4 K

d

5

____~_

Start Finish Water

type

Depth

(m)

5 20 35

K

d

K

__. 10 m

0.15

Sm

0.18

15 m

0.10

3m

0.45

8m

0.18

15 m

0.10

Coastal

Coastal

2-7

oA of surface 10.0-2.0 0.8-0.003 0.06 -dark

3

Coastal

I

illumination 7.5 0.4 0.02

12.5 I.5 0.2

At the end of the incubation periods, all the jars were wrapped in aluminium foil, brought to the surface, and rapidly transported to the laboratory. The corals were then washed in running sea water in the dark for 1 h to remove occluded radioisotopes from the skeleton. Two 2%ml samples of the incubation water were taken, one for the estimation of specific radioactivities, the other for immediate analysis of dissolved oxygen content by a modification of the Winkler method. The volumes of the corals were determined after washing by measuring water displacement in a graduated cylinder and they were then blotted and weighed wet. Subsequent preservation was either by fragmenting and placing in screw-capped 2%ml bottles with a 2 : 1 methanol : chloroform mixture, or by immediately drying in an oven at 1% “C, leaving there overnight, and then wrapping in foil before sealing into heavy duty

PHOTOSYNTHESIS

polythene

bags for transportation.

AND

CALCIFICATION

The

latter

samples

169

IN CORALS

were weighed

dry

before

packing. RADIOISOTOPE ANALYSES

The dried corals were extracted overnight with cold methanol : chloroform then extraction of these and also of the liquid preserved corals was completed

and with

three changes of hot solvent left 15 min between changes. All the samples were oven dried and weighed after extraction; they were then all wrapped in foil, placed in heavy duty polythene bags, and broken into small fragments with a hammer. These fragments were then ground to the consistency of coarse sand in a pestle and mortar. In some cases granitic pebbles were found in the skeletons: these were removed, weighed and the coral weight adjusted accordingly. De-calcification of 1 g subsamples of the ground material was carried out with cold concentrated HCI in 10 ml centrifuge tubes: the acid was added a drop at a time and the tubes spun at 3000 rpm in a bench centrifuge between additions to prevent excess frothing. When de-calcification was completed, the organic residue was centrifuged and washed twice with distilled water, the washings being combined with the initial acid digest. The acid digests were made up to standard volume and aliquots added to excess saturated ammonium oxalate in centrifuge tubes. This mixture was then made alkaline with 0.88 N ammonia solution, using bromocresol green as an indicator, the samples heated to 70 “C in a water bath, cooled, and centrifuged. The precipitates were rinsed twice with hot distilled water and the washings added to the original supernatants. These procedures gave four fractions for each coral sample namely, I ) the methanol: chloroform soluble fraction, of which two 0.25 ml aliquots were dried down on planchets with wax pencil rings around the perimeter to prevent edgecreep; 2) the organic residue after de-calcification, all of which was spread evenly on a planchet and dried; 3) the calcium oxalate precipitate, all of which was spread evenly on a planchet and dried; 4) the supernatant from oxalate precipitation, of which two 2-ml aliquots were dried down on planchets in four 0.5 ml applications. These were counted with a proportional gas-flow counter. Samples for the assay of the specific radioactivities of the incubation waters were obtained as follows; for 45Ca, oxalate precipitates from 2 ml aliquots of the sea-water samples were obtained as described for the acid digests and planchets prepared as in 3) above; for 14C, 1 ml/aliquots of the sea-water samples were added to centrifuge tubes containing 1 ml saturated barium hydroxide solution and the resulting precipitate washed twice with hot distilled water before being quantitatively transferred to a planchet and dried. All the planchets were weighed before and after application of the fractions, and the areas covered by these were determined. Subsequent count rates were corrected for self absorption losses according to the cross-sectional densities thus obtained. Control analyses of samples where only one of the two radioisotopes was present

EDWARD

I 70

indicated

very little contamination

A. DREW

of organic

fractions

by 45Ca or of calcium

pre-

cipitates by 14C, except in the case of the water analyses where barium carbonate precipitates prepared as above from water with only 45Ca contained significant amounts of radioactivity. This contamination was found to be constant and appropriate corrections were applied to the counts from water which also contained 45Ca.

from

MEASUREMENT

PHOTOSYNTHETIC

OF RESPIRATORY

CONSUMPTION

AND

i4C containing

precipitates

PRODUCTION

OF

OXYGEN

Measurements of oxygen consumption by corals in foil-wrapped 475 ml sealed jars were made in a laboratory aquarium with running sea water at a constant temperature of 22 “C. Sub-samples of the water in those jars were taken at the end of the incubation period as well as initial control sub-samples from the primary water source. Several jars were set up at the start of each experiment and a separate one analysed at the end of each successive hour. The sub-samples were taken as soon as the lid had been removed; 28 ml screw-capped jars were carefully submerged in the incubation jars and the lids screwed on underwater to exclude all air bubbles. Dissolved oxygen determinations were then made using a slight modification of the Winkler method. The volume and weight of the coral samples were determined before they were dried overnight at 150 “C and their dry weights determined. A similar method was used to determine the production of oxygen in photosynthesis by the corals incubated in the light in 14C experiments in situ on the reef. and in situ dark controls were analysed to provide further respiration data. Control incubation jars without corals were used to give the initial oxygen content of the sea water; there was no change in dissolved oxygen in these control jars in the light during the incubations. Initial water usually contained 4.8 ml/l dissolved oxygen or 2.3 ml per incubation jar; oxygen content never fell below 50 “/;; of this in any experiments which were up to 5 h duration. In calculations based on these oxygen determinations, the equivalence of oxygen production/consumption to the corresponding carbon metabolism was estimated assuming a respiratory/photosynthetic quotient of 0.86 since the major metabolic substrate involved was probably glycerol (see Muscatine, 1967; Muscatine & Cernichiari, 1970; and also evidence presented later in this paper). This gives an equivalence of I ~1 of oxygen for 0.47 pg of carbon.

RESULTS PHOTOSYNTHESIS

Carbon fixation profiles determined from the amounts of 14C fixed in the light by the three species used are shown in Fig. 1. In all cases there was a marked reduction with increased depth, although this was not as great as the decrease in light intensity (see Table II). The data are for pg carbon fixed/g total weight/h. The amount of

PHOTOSYNTHESIS

AND

ACROPORA

IN CORALS

MILLEPORA

I 5

Fig. 1. Variation

CALCIFICATION

I

1

I 20

I

171

GONIASTREA

I

I 35

of gross photosynthetic rates, with depth measured by 14C and oxygen in three coral species (range of replicates indicated by vertical bars).

methods,

animal

tissue was probably in the region of 2 y0 total weight for Acropora and Milsince residual organic matter after methanol : chloroform and cold acid extraction amounted to 1.1 % of the total weight. Goniastrea, with only 0.5 “/:, organic residue, would have about half that total animal tissue per unit total weight, which to a large extent explains the considerably lower photosynthetic rates found in this species. Carbon fixation rates per unit organic residue are given in Table 111. lepora,

TABLE

Carbon Depth

fixed/unit

organic

residue

III

in three coral species,

(m)

,ig carbon/mg Acropora ________~

5

20

1.74) _ , 1.74

measured

by the 14C method

residue/h

Milleportr

Goniastrea _

--

‘.20’ 1.12 1.04 I

o’68’ 0.69 0.70 j

0.561 0.541 o.55

0.30 \ 0.33 j o.32

.-.

35

Values for gross oxygen production (increase over initial in the light plus loss in the dark) during the 14C incubati ons are also shown in Fig. I, after conversion to equivalent ,ug carbon. The values were very similar in all cases to those calculated from the amount of 14C fixed, and it therefore appears that, for corals, the t4C method

172

EDWARD

measures

gross photosynthetic

carbon

A. DREW

fixation

within

the limits of experimental

error

and tissue variability. Values for oxygen production have also been calculated per g total weight per h; however, to allow direct comparison with values for similar organisms determined by Yonge, Yonge & Nicholls metabolism per unit volume of the specimens have compared similar.

(1932) values for the oxygen also been calculated and are

with their data in Table IV; the values for the two series of experiments

are

TABLE IV Comparison

of gross

photosynthetic rates and dark respiration rates/unit volume and Low Isles, Great Barrier Reef (Yonge, et al., 1932). /cl oxygen/ml

coral

of coral

volume/h Low Isles (29.5 4m)

Eilat (21 “C, 5 m deep)

at Eilat

C.

__ Dark

respiration

Millepmw

18.5

Goniastretr

5.6

16.6

Fnricr

Gross

6.3

photosynthesis

Milleporu

37.5

Goniastrecr

16.3

26.

Focia

I

15.3

RESPIRATION

The time courses for the consumption of oxygen by Millepora and Acropora in the dark in laboratory experiments are shown in Fig. 2. Data for Millepora dark treatments on the reef are also shown and are very similar to the laboratory results; in situ data for Goniastrea are also included. In an experiment using pieces of Acropora from a similar

tabular

colony

growing

at 35 m depth a much lower rate of respira50

100

/ /J / i/.A /’ /+

2

0" i

:

*

?Y u ?

__4--*

_--i

/

2

3

4

5

hours

Fig. 2. Time courses of oxygen consumption in dark respiration by three coral species in the laboratory and also in situ on the reef: Ml, Millepora in laboratory; M2, Millepora in sea; A, Acropora in laboratory; C, Goniastrea in sea.

PHOTOSYNTHESIS

tion

was recorded

than

AND

CALCIFICATION

from the 20-m samples

173

IN CORALS

(4.0 ~1 as compared

with

17.0 ~1

0,/g/h); this is possibly an adaptation to growth in dimmer light although its immediate cause may be the much denser skeleton and hence lower organic matter content per unit weight. The 20-m samples had an average density of 1.54 g/ml but the 35-m samples 2.01 g/ml; of the other two species used, Millepora had the lowest density, namely 1. I3 g/ml, whilst the density of Goniastrea was I .70 g/ml. The respiratory rates determined at Eilat are compared with those of Yonge, Yonge & Nicholls (I 932) in Table IV, and again the values are similar for the two places. The use of a respiratory/photosynthetic quotient of 0.86 for conversion of oxygen metabolism to carbon values, based on the probability that glycerol is the major metabolic substrate involved, is supported by analysis of the soluble carbohydrate components of the corals. Using the gas-liquid chromatography techniques described by Holligan & Drew (1971) the only compound detected in the methanol: chloroform extract of Acropora was chromatographically identical to glycerol and this was present at a concentration of about 3 “/<;total organic matter (residue x 2). NET CARBON

FIXATION

This

has been calculated from the 14C fixation data by subtraction of respiratory carbon losses as determined from both in situ experiments and in the laboratory, and also from the determinations of increased dissolved oxygen in light incubation jars on the reef. There is good agreement between the two methods, even in the case of the low rates recorded for Goniastrea, and the data are given in Table V.

TABLE

Net carbon

Depth Cm)

fixation

Acroporn

5

~’ 12.4 1 9.8 II.4 12.1

20

~. 1.0 i 1.5 ! 2.2 1 0.9

35

-3.5 ~ 5.9 i -4.5 --3.4

* * 4.3

-4.2 ~ 4.4

i -

4.3

from

‘“C and

77.9 -1 10.6 i

“C

02

1-9.3

-1.2) -,.9 -2.6 1

r0.3 1 1~1.1 j 0.9 (

-2.1 -4.7

-3.01 ~ 3.3 -3.5 j

1 -3.4 J

both

Goniastrecr

14C

02

-:mg.g \ f 9 ’7 -t10.6J

-

calculated medium.

Milleporu

‘V

02

V

rates (ug C/g total W/h) in three coral species oxygen data: * 14C not present in incubation

t3.01 ~. 2.6)

+2g ’

-0.41 __o . 6 -0.7 I

2.01 1 1.2)

’ 0.4 \ IO.71

1.7

. 0.6

174

EDWARD

The daily equivalent already

carbon

balances

A. DREW

for these corals

of 12 h full light photosynthesis determined.

Although

are shown

the measurements

were made

of underwater illumination, all three corals showed to at least 10 m depth (see also Table VI) where

Fig. 3. Net carbon

babance

of three

in Fig. 3, assuming

per day and 24 h respiration

coral species at various oxygen metabolism.

under

the

at the rates

poor conditions

net carbon fixation down ambient light energy was

depths

calculated

from

both

“C

and

about 5 % of that at the surface. With the excellent underwater illumination usually prevailing on this and most other coral reefs, this proportion of surface light penetrates to between 20 and 45 m for waters of Jerlov’s Oceanic Types 11 and I respectively, so that such corals would be autotrophic conditions. TABLE

Compensation

depths

on a daily carbon

to considerable

depths

such

VI

accretion basis for three I‘% and oxygen data. Compensation

coral

depth

species,

as indicated

(m)

‘-T

Oxygen

Acropora

15

12.5

14

Millepora

II

8.5

IO

8

II.5

IO

Goniasirea

under

--__

Mean ____---

by both

PHOTOSYNTHESIS CALCIFICATION

Although calcification

AND

CALCIFICATLON

175

IN CORALS

RATES

one aim of these experiments was to determine the variation in rates of with increased depth in the various types of coral, certain factors have

made the results less easy to interpret amounts of 4sCa actually incorporated

than was expected: however, although the and detected were rather low, significant

incorporation was detected in all experiments, and in all cases there was more incorporation in the light than in the dark. Values for each incubation are set out in Table VII; they show considerable variation between replicate incubations and this tends to obscure changes with depth. Rates of calcification did not seem to be reduced as much as those for carbon fixation at increased depth. Except for Goniastrea, they were all lower than the rates reported by Goreau & Goreau (1966) for similar material at shallow depths in Jamaica, which are also shown in Table VII. This could well be due to the poor submarine illumination conditions at Eilat. TABLE VII

Calcification rates in three coral species measured at Eilat, and compared with data from Jamaica (Goreau & Goreau, 1959): nitrogen content of specimens calculated assuming that total organic matter was twice weight of organic residue after decalcification, and that nitrogen represented I I O,, of the organic matter. Depth

Eilat

Jamaica

(m) ,(g Ca/mg

/‘g Ca/g/h __

_______

A croporcr 5 20 35 Dark Dead

2.8, 9.1 8.0,2.4, 5.9, 1.9, 8.9, 4.6, 7.9 (5.9)

(5.8) 15.1 (7.1) 2.1 (3.2) 2.2 (3.0)

2.4 3.0 1.3 1.3 2.5

N/h

maximum minimum average dark

- 7 I .5 - 15.0 - 23.2 4.9

Milleporcr 73, 49 36,43 40,43 12,20,

(6/) (40) (42) I6 (16)

25.4 16.6 17.4 6.6

Gonicrstren 5 20 Dark Dead

,rg Ca/mg ____~_ Acroporo

5.6, 2.8, 2.7, 2.2, 3.9,

Milleportr 5 20 35 Dark

N/h

Sun Cloud Dark

- 38.9 - 23.8 -. 4.7

Goniastren 15.0, 8.2 (I 1.6) 9.3, 10.3 (9.8) 4.2, 2.8 (3.5) 9.3 (9.3)

Ii.6 9.8 3.5 9.3

Sun Dark

- 10.2 - I.5

In the experiments in which the contribution of purely physical isotope exchange to the incorporation of 45Ca was measured with corals killed underwater with formaldehyde, 45Ca incorporation was always greater than in corresponding dark treatments (see Table VII). These results are similar to those obtained by Goreau &

EDWARD

176

Goreau

(1961) who showed

A. DREW

that the presence

of a dead coenosarc

over the coral

skeleton had no effect on the exchange reaction. In the present study it has, therefore, been assumed that such exchange in living corals occurs only slowly, representing a maximum of 0.5 % of total 45Ca deposited according to those authors; no correction

has been made for this. DISCUSSION

The experiments have shown that in situ 14C and 4sCa experiments can readily be carried out on hermatypic corals to considerable depths on reefs using the techniques devised for experiments on macrophytic marine algae (Drew, 1973). The suitability of the methods used for preservation of specimens containing radioactivity is important in studies which may be carried out a long distance from the analytical laboratory. There was no apparent difference between results obtained with the two methods tested; the results of replicate treatments preserved differently (in methanol : chloroform or dry) are shown in Table VIII. In view of this, immediate drying at a fairly high temperature (about 150 “C) is probably the more suitable technique if facilities are available, since it saves the transportation of heavy bottles and potentially dangerous liquids. For the purposes of this work, methanol : chloroform extraction could be dispensed with, although any detection of glycerol in dried material may be prevented due to its relative volatility. TABLE VIII Comparison

of photosynthetic rates (‘?Z method) and calcification rates determined of Millepora preserved either in methanol : chloroform or by rapid drying. Methanol chloroform

:

Dried

(/lg C/g/h)

5m 20 m 35 m

Calcification 5m 20 m 35 m

~~(%,

Solvent

_____ Photosynthesis

Dried

in samples

15.2 1.6 5.3

Il.9 9.2 4.8

118% 121 “/, 90 O?,

49 43 43

I I 6 “<,

(pg Ca/g/h) 73 36 40

67 “/;, 108 2,

The results of these experiments show that, despite the unusually poor conditions of submarine illumination at Eilat during the period concerned (April 1971). considerable rates of both carbon and calcium accretion could be detected. Miflepora and Acropora showed very similar rates of photosynthesis at all depths despite the fact that the former was taken from only 3 m; the latter, from 20 m depth, could

PHOTOSYNTHESIS

AND

CALCIFICATION

IN CORALS

have been expected to be more adapted to the lower illumination at greater These two branching corals have already been shown by several workers

177

depth. to be

rapidly growing corals, whilst the massive types, such as Goniustrea used in this work, always have lower metabolic rates. This difference is usually attributed to their higher skeleton/tissue ratio, a feature borne out by data in Table III in which the three species are shown to photosynthesize in terms of unit weight of organic matter.

at more comparable rates when expressed Nevertheless, even the Goniastrea colonies

showed considerable carbon accretion in these experiments, at least in the shallower depths. Gross photosynthetic rates determined with the 14C method were somewhat lower than those reported by Goreau (1963) for comparable material in Jamaica. Thus, Acropora fixed only about 8.0 pg C/mg N/h at Eilat compared with 10.5 pg in Jamaica: the data for Miffepora were 6.7 pg and 9.7 pg respectively. This was again probably due to the lower light intensities at Eilat. Although Yonge, Yonge & Nicholls (1932) suggested that oxidation of the mucus secreted by corals in closed containers might interfere with respiration measurements, Franzisket (1970a) showed that this mucus had no effect over I2 h in his experiments: enhanced bacterial metabolism did effect oxygen consumption rates after that time. In the present experiments, in which corals were used for maximum durations of 5 h in sealed vessels and in which the animals were never removed from water nor excessively handled during pre-experiment operations, it is equally unlikely that any such artefacts affected the results. The rates of respiration reported are high in relation to photosynthetic rates (see below) when compared with completely autotrophic organisms such as macrophytic green algae in which respiration is usually less than 20 y0 of photosynthesis under moderate illumination. Respiration in these corals was, however, adequately compensated by a high photosynthetic rate so that they could be autotrophic over a 24-h period in shallow water, to about 10 m depth in these experiments in turbid water, and perhaps to 30 m in clear water. This is contrary to the findings of Yonge, Yonge & Nicholls (1932) at Low Isles even in very shallow water, although that water was probably even more turbid than that at Eilat and was certainly considerably warmer; data presented in Table IV show that respiration was 49 7, of gross photosynthesis in Millepora and 32.5 y/, in Goniastrea at Eilat, whereas comparable values 64 o/oand 41 ‘/” (Fauiu) were found at Low Isles, and this could explain the differences in autotrophic potential in shallow water. Indeed. Yonge et al. found a deficit of only I8 pg C (38 ~10,) per ml of coral sample per day in one 24-h experiment with Fuviu, and an excess of 5.3 pg C (I 1.3 ,ul 0,) in a second experiment. Their data for Milfepora show a deficit of about 176 pg C (386 ~1 0,) per ml per 24 h, a very high value which is not consistent with their other data for this species nor with those from many of the other species they used. There are several other conflicting reports concerning the ability of corals to survive by virtue of the photosynthetic activities of their zooxanthellae, such as that of Franzisket (1970b) who found that most hermatypic corals completely deprived

178

EDWARD

of animal and

food grew normally

expelled

directly

all their

contrary

A. DREW

in the light whereas they rapidly

zooxanthellae,

even

to the results of Yonge

if animal

& Nicholls

food

atrophied

in the dark

were available.

(1931a, b) who found

This

is

that their

material survived well in the dark provided they were fed but rapidly atrophied when starved of animal food in the light. Goreau (1964) reported that shallow water corals on Jamaican reefs, caused to expel their zooxanthellae by the greatly reduced surface salinities associated with the rains accompanying Hurricane Flora, continued to grow normally and took a long time to re-develop their algal component. It appears, therefore, that corals are adaptable organisms which specialize in the type of nutrition appropriate for their area of growth - efficiently carnivorous where the water is turbid and relatively rich in zooplankton, but autotrophic on clear water reefs with little plankton. The degree and speed of adaptation when conditions are changed either naturally or experimentally probably differ between species and, according to Franzisket (1970b), there may be some correlation between an effective autotrophic nutrition and small polyps which are neither as effective at carnivorous feeding nor usually as metabolically active. Irrespective of the autotrophic status of a coral community, the zooxanthellae are always useful in their role originally proposed by Yonge (193 I), that of waste product removers. Further experimentation is required to establish the exact relationship between calcification rates and illumination: the results presented here, obtained at levels of illumination at which maximal calcification rates would not be expected. suggest that even dim light has a considerable stimulatoryeffect’. Reduction in rate withdepth is certainly not as great as reduction in ambient light intensity or of photosynthesis. Goreau & Goreau (1959) showed that cloud cover only reduced calcification rates by about 40 x, whereas the available light energy may be assumed to have been reduced at least fourfold under such conditions, so that even at the upper end of the illumination scale there is not a direct quantitative relationship between light intensity and calcification

rates.

ACKNOWLEDGEMENTS

This work was financed by a grant from the Carnegie Trust for Scottish Universities. Considerable assistance was rendered in the field by the staff and visiting scientists at the Marine Biological Laboratory of Jerusalem, situated close to Eilat, and I should especially thank Dr Francoise Lafargue who accompanied me on most of the underwater work. The Israeli authorities kindly granted me permission to take the necessary corals in this area which is strictly protected. Coral identifications were verified by Mr B. Rosen, University of Newcastle. ’ The demonstration by Pearse & Muscatine (Bid. Bull. mrrr. bid. Lob., Woods Hole. 1971,Vol. 141, pp. 350-363), that calcification in Acropora branch tips is enhanced by products of algal photosynthesis translocated there from lower down the branches is consistent with this observation. since there is still some photosynthesis in dim light.

PHOTOSYNTHESIS

AND

CALClFICATlON

IN CORALS

179

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