PROCESSES OF ORGANIC PRODUCTION ON CORAL REEFS

Bid . Rev . (1977)~ 52. PP . 3 0 5 3 4 7 BRCPAH 52-10

Printed in G e n t Britain

PROCESSES OF ORGANIC PRODUCTION ON CORAL REEFS

BY JOHN B . LEWIS

Montreal. Quebec

(Received 21 October 1976. revised 11 March 1977)

The Redpath Museum and the Marine Sciences Centre. McGill University.

CONTENTS . . . . . . . . . . . . I Introduction 305

I1 . Methods of study . . . . . . . . . . . . 306 I11 . Rates of primary production . . . . . . . . . 3 1 0 IV . Sources of primary production . . . . . . . . . 311

( I ) Macrophytes . . . . . . . . . . . 311 (2) Calcareous algae . . . . . . . . . . . 313 (3) Boring filamentous algae . . . . . . . . . 314 (4) Marine grasses . 314 ( 5 ) Phytoplankton . 315

. . . . . . . . . .

. . . . . . . . . . (6) Zooxanthellae . . . . . . . . . . . 315

V . Nutrient flux . . . . . . . . . . . . 317 ( I ) Phosphorus . . . . . . . . . . . . 317 (2) Nitrogen . . . . . . . . . . . . 318

VI . Detritus . . . . . . . . . . . . . 320 VII . Zooplankton . . . . . . . . . . . . 322

IX . Sessile invertebrates other than corals . . . . . . . . 324 X . Fish . . . . . . . . . . . . . . 325

XI . Trophic relationships . . . . . . . . . . . 326 XI1 . Coral growth . . . . . . . . . . . . 329

XI11 . Growth and erosion of reefs . . . . . . . . . 329 ( I ) Carbonate production . . . . . . . . . . 329 (2) Boring organisms . . . . . . . . . . . 330 (3) Predators . . . . . . . . . . . . 331 (4) Pollution . . . . . . . . . . . . 331

XIV . Hydrographic conditions . . . . . . . . . . 331 XV . Discussion . . . . . . . . . . . . . 333

XVI . Summary . . . . . . . . . . . . . 335 XVII . Acknowledgements . . . . . . . . . . . 336

XVIII . References . . . . . . . . . . . . . 337 XIX . Addendum . . . . . . . . . . . . . 347

. . . . . . . . . . . VIII Microbial production * 323

I . INTRODUCTION

Perhaps the most logical beginning for the theme of production on coral reefs is the work of Darwin (1897) who was ‘ ‘ struck with astonishment’’ when first observing an atoll in the Pacific Ocean . His enthusiasm for coral reefs increased during his voyage and he made frequent references to the variety of animals that flourished on them .

306 J. B. LEWIS This abundance and exuberance of life on coral reefs has been reported in a general way by numerous authors before and since Darwin. Such studies as those of Gardiner (1898), Vaughan (1914), Mayor (1924a, b), Crossland (1928) and Edmondson (1928) commented upon the richness of the fauna to be found on reefs. The early work consisted of both field and experimental studies and was concentrated upon relationships between reef form and the environment, with emphasis upon such critical factors as temperature, exposure, sedimentation and water turbulence. Subsequent interest in coral reefs by both geologists and biologists led to the establishment of field stations such as those at the Palao Tropical Biological Station in the Pacific and the Dry Tortugas Laboratory of the Carnegie Institution in the Atlantic. Much of the early work has been amplified in a series of papers from the Great Barrier Reef Expedition of 1928-9 and summarized by Yonge (1940). Later reviews of the biology and ecology of coral reefs have beenpublished byWells (1957),Yonge (1963a, 1973)andStoddart (1969).

The first quantitative studies of primary production emerged from the pioneer work of Sargent & Austin (1949, 1954) and concerned the mechanism whereby atolls and reefs develop high rates of organic production in nutrient-poor and relatively barren oceans. Their studies at Rongelap Atoll in the Pacific showed that productivity on the reefs was considerably higher, per unit area, than that of the surrounding waters. Not only was the rate of primary production higher than expected on the basis of nutrients available, but the biomass of plankton carried on to the reefs by currents was grossly inadequate to support the animals living on the reefs. The investigations of Sargent & Austin were soon followed by similar studies by Odum & Odum (1955) and by Kohn & Helfrich (1957) who confirmed the general conclusions reached by Sargent & Austin. I t is apparent that rates of primary production on coral reefs compare favourably with other highly productive parts of the sea and with those on land. The performance of shallow-water-reef systems as primary producers is thus of great interest and practical importance, and productivity is a central theme currently being investigated by coral-reef biologists.

There has been a marked increase in interest in the biology of corals and coral reefs within the past ten years. This is reflected in the organization of two international symposia devoted entirely to the study of corals and coral reefs. The first was held in 1969 in Mandapam, India and the second on the Great Barrier Reef of Australia in 1973. The published proceedings of these symposia include original papers on many aspects of reef ecology, geology and biology. In addition, the publication of a treatise on the biology and geology of coral reefs (Jones & Endean, 1973 a, b, 1976) has made available reviews of current knowledge of reefs from many areas of the world.

11. METHODS OF STUDY

The basic technique for estimating organic production on reefs has been that of flow respirometry, whereby changes in oxygen concentrations have been monitored in the water flowing over a reef. This method measures community metabolism and depends on the flow of unidirectional currents across a reef. Oxygen concentration in the water is determined by the Winkler method or by oxygen electrodes.

Organic production on coral reefs 307

Fig. I . Simplified profile of a coral reef showing positions of sampling stations for flow respirometry studies.

I I I I I I I I I I I

16.00 20.00 24.00 04.00 08.00 12.00 16.00 20.00 24.00 04.00 08.00 12.00

Fig. 2. Diurnal curves of oxygen concentrations in water flowing over a coral reef during flow respirometry studies. Source: Kohn & Helfrich, 1937.

Net photosynthesis and respiration of the reef can be measured by determining the oxygen content of the water upsteam and downstream simultaneously (Fig. I). The oxygen increase between stations during the day is the net photosynthetic production of the community while the oxygen decrease between stations at night is the cormnu- nity respiration. By taking a series of diurnal measurements one can obtain estimates of the daily variation in production. A graph of diurnal variations, such as that shown for a Hawaiian coral reef in Fig. 2, indicates a photosynthetic maximum just after midday and a stable level of respiration at night. The approach leads to estimates of gross and net community production, turnover rates, and efficiency of production.

308 J. B. LEWIS The problems of accurate and reliable measurement of rates of production by the

flow respirometry method have been discussed by Gordon & Kelly (1962), Owens (1974) and Westlake (1974). The major sources of error lie in short-term fluctuations in the concentration of dissolved gases. These fluctuations may be due to surface roughness of the water crossing the reef, to temporal variations in tidal height and current velocity, and to wave and wind velocity. Thus, in following changes in dissolved oxygen, the exchange of gas between the air and water and the rate of mixing must be determined or estimated. Temperature measurements should be made at the same time. Many authors recommend that measurements of dissolved oxygen should be made as frequently as possible at each station and that a series of observations over several 24-hour cycles be made at different times of the year.

The principles underlying the procedure of flow respirometry seem correct and the method has some considerable advantages over measurement of rates of production in an enclosure. Observations on natural changes in water flowing over a reef can be continued over long periods whereas experiments in enclosures are limited by temporal changes in concentrations of metabolites. Since rates of metabolism are affected by external changes, the method of flow respirometry is a better measure of the natural behaviour of the organisms on a reef.

Provided that suitable corrections are made to initial measurements of oxygen concentration, flow respirometry is probably the most reliable method of determining rates of community production on a reef. Thus, the simple flow methods used by Sargent & Austin (1949, 1954) and Odum & Odum (1955) have been refined subsequently and each successive study has led to methods of increased reliability. Cor- rections for the effects of oxygen exchange across the air-sea interface have been applied by Kohn & Helfrich (1957) and by Odum, Burkholder & Rivero (1959). Gordon & Kelly (1962) calculated specific transfer coefficients for oxygen diffusion and multi- plied saturation deficits by the average value of transfer coefficients for regular sample- time intervals. These corrections together with careful measurements of current velocity were applied to the data on oxygen concentration. Kinsey & Domm (1974) also made corrections for diffusion, tidal cycles and current velocity in a reef area in Australia. Details of methods and calculations of correction factors are provided by Owens (1974).

While rates of production on reefs are usually measured initially in terms of oxygen concentration, these are converted by most authors to carbon equivalents. Assuming that the conventional equation for photosynthesis (CO, + H,O = CH,O + 0,) is valid, then CH,O stands for organic matter produced by photosynthesis. It follows that each 30 ml of oxygen (N.T.P.) produced is equivalent to 16 mg of carbon fixed as organic matter when the photosynthetic quotient is equal to 1.0 (Sargent & Austin, 1954). However, the elaboration of substances such as protein and fat leads to higher values. Pillai & Nair (1972) argued that a quotient of 1-25 was more suitable while Drew (1973) has used a quotient of 0.86 on the assumption that the major metabolic substrate involved in corals was glycerol. Conversions by Westlake (1963) were based on photosynthetic quotients of 1-2 (average values) and of 1-25 for tropical communities. There is thus a problem in comparing oxygen uptake with that of

Organic production on coral reefs 309 carbon and comparative values are affected by the choice of the photosynthetic quotients.

Besides oxygen, determinations of the various forms of carbon dioxide (free carbon dioxide, carbonate and bicarbonate) may be used to measure production. Smith (1973) and Smith & Marsh (1973) have used the marine carbon dioxide system to monitor organic production in water flowing over a reef at Eniwetok Atoll. Smith et al. (1971) and Smith & Pesret (1974) investigated the processes of carbon dioxide flux at Fanning Island in the Line Islands. By measuring pH, total alkalinity and applying suitable corrections, Smith (1973) was able to calculate carbon dioxide changes due to production and respiration of a reef community as well as to estimate rates of calcification.

The problems of measuring organic production by the carbon dioxide method are more complex than by means of oxygen, since a number of factors affect the solubility of carbon dioxide. The carbon-dioxide content may be influenced by the total alkalinity, the hydrogen-ion activity and the complexity of the marine carbon-dioxide buffer system. In addition, the slow rate of gas exchange at the air-sea interface as well as the short-term fluctuations due to water turbulence and mixing, characteristic of flowing waters, can influence carbon dioxide concentrations. Nevertheless, pH is a most sensitive property for detecting variations in the system and the carbon-dioxide method does have the advantage of estimating calcium-carbonate production as well as community photosynthesis and respiration. Details of the methods of calculation are provided by Vollenweider (1974) and by Smith & Pesret (1974), and problems in the methodology are discussed by Smith (1973). The carbon dioxide method may be seen as a matter of choice, either replacing oxygen or as a means of checking results by other methods.

Attempts have also been made to measure production of benthic organisms in situ on the reef and in the laboratory. Thus Odum & Odum (1955) enclosed reef surfaces in glass vessels and determined the change in oxygen content at suitable intervals. Results by this method were compared with data from flow respirometry by Odum & Hoskin (1958), who found that metabolic rates from dark and light bottle measurements were less than the values from diurnal curve methods.

Production rates of corals themselves have also been measured in situ and in the laboratory. Yonge, Yonge & Nicholls (1932) and Odum & Odum (1955) enclosed corals in situ and found that rates of oxygen production by zooxanthellae were approximately balanced by respiration rates over a diurnal cycle. Kanwisher & Wainwright (1967) and Roffman (1968) measured respiration and production by corals in the laboratory with oxygen electrodes and found oxygen excesses in varying amounts produced by both Atlantic and Pacific corals.

As noted above, changes in parameters in enclosed vessels reflect alterations within the enclosures rather than within the community and hence are subject to considerable error. Rates of oxygen exchange of enclosed corals, for example, will include respiration of attached epifauna and boring organisms within the coral skeleton and hence tend to be overestimated.

Estimates of primary production by corals by the 14C method have been calculated by Pillai & Nair (1972) and Drew (1973) using dark and light bottles. The former

3 1 0 J. B. LEWIS authors found that net values of 14C incorporated in corals were less thanvalues obtained by the oxygen method, and Drew concluded from in situ studies that gross photosynthesis could be measured by this method.

In order to evaluate the methodology of production in enclosed vessels Littler (1973) used a number of methods to measure production of reef-building coralline algae. He found that 14C results were somewhat higher but not significantly different from results obtained by oxygen and pH methods. Littler concluded that oxygen and pH electrode methods were more useful and reliable than 14C methods where high sen- sitivity was not required.

Sournia (1976) also compared rates of production of oxygen on a reef in French Polynesia by the flow method and by the light and dark bottle technique. He concluded that the two techniques gave similar results but pointed out the advantages of combining two or more methods when measuring production on such complex systems as coral reefs. This view appears to be reflected in the opinions of most other workers in reef-production ecology.

Thus, a number of methods are available for measuring production on reefs. Flow- respirometry methods are concerned with community metabolism of the reef while studies in situ and in the laboratory have been used to elicit the role that corals and other benthic organisms play in reef production.

111. RATES OF PRIMARY PRODUCTION

A comparison of rates of primary production on coral reefs shows most values between about 300-5000 gC/m2/yr. These are estimates of gross production in waters flowing over the reefs. Estimates from a number of regions are presented in Table I." The reason for the difference in rates lies apparently in the nature of the reef surface studied. For example, rates of primary production appear to be higher over lagoon areas covered by algae and marine grasses than over reefs dominated by coral growth. The highest values reported are those from a Hawaiian fringing reef of I I 680 gC/m2/yr by Gordon & Kelly (1962). In contrast, the estimates of gross production of the ambient waters in the vincinity of reefs are very low: 21-37 gC/m2/yr for Hawaii (Doty & Oguri, 1956); 28 gC/m2/yr at Rongelap (Steemann-Nielsen, 1954); 50 gC/m2/yr in Barbados (Beers, Steven & Lewis, 1963).

On many reefs the ratio of production (P) to community respiration (R) was greater than I . The highest P/R ratios were found over areas covered by algae and the marine grass, Thalassia testudinum Konig. Nevertheless, it may be seen from Table I

that respiration exceeded production in Puerto Rico (Odum et al., 1959), Hawaii (Gordon & Kelly, 1962), and in the Indian Ocean (Nair & Pillai, 1972). Thus all reefs are not 'autotrophic' in the sense that they produce more organic material than they consume.

The normal range of oceanic net primary production is estimated by Riley (1970) * In so far as is possible, production values are stated in gC/me/yr throughout this review. Data

presented by authors in other units have been converted by factors contained in the International Biological Programme report by Winberg (1971).


Table I. Comparison of estimates of primary production of coral reefs, atolls and seagrass beds made by d@went authors

Gross Community production respiration

Locality (gC/m'/uear) (gC/m*lyear)

Hawaiian coral reef, 7300 12370

Fringing coral reef, North 2427 2200

Eniwetok Atoll, Marshall 4200 4200

Coconut Island

Kapaa, Hawaii

Islands El Mario reefs, Puerto Rico 4450 4100

Eastern Reef, Rongelap Atoll, 1250 1090

Kavaratti lagoon, Laccadives 4715 3482

Bimini lagoon, British 319 20.5

Kavaratti reef, Laccadives 2250 880

Marshall Islands

West Indies

Turtle grass bed, Long Key, Florida

Turtle grass bed, West La Gata reef, Puerto Rico

Turtle grass bed, Isla Magueyes, Puerto Rico

Eniwetok Atoll, algal flat One Tree Island, lagoon reef Eniwetok Atoll, coral algal flat Guam, reef flat Eniwetok Atoll, windward

Eniwetok Atoll, algal flat reef flat

3880

980

4234 1387 2190 6900 3285

5329

2740

1290

1500

2190 1314 2190 2600 2190

2190

1'1

I '0

1'1

1'1

1 '3

2'5

1 '4

0.8

0.9

J '9 1'1 I ' 0

2.6 I '5

2.4

Authors

Gordon & Kelly (1962)

Kohn & Helfrich (1957)

Odum & Odum (1955)

Odum, Burkholder &

Sargent & Austin (1954)

Qasim & Sankaranarayanan

Odum & Hoskin (1958)

Qasim & Sankaranarayanan

Rivero (1959)

( 1970)

( 1970) Odum (1957)

Odum, Burkholder & Rivero

Odum, Burkholder & Rivero

Smith & Marsh (1973) Kinsey (1972) Smith & Marsh (1973)

(1959)

(1959)

Marsh (1974) Smith (1974)

Smith (1974)

to be between 50 and 150 gC/m2/yr. Production in inshore areas and in regions of upwelling may be more than ten times greater than oceanic values. When rates of primary production on coral reefs are compared with those of other marine systems it is apparent that they may be as high as in the most fertile waters. Values of primary production for oceanic, benthic and terrestrial systems have been tabulated by Crisp (1975) and are reproduced in part in Table 2. It may be seen that production on coral reefs and tropical marine grass beds is as high as primary production in the Peru Current, and greater than the production of sugar-cane in Java, to take a terrestrial example. Westlake (1963) concluded that the most productive marine benthic plant communities of all were to be found on coral reefs.

IV. SOURCES OF PRIMARY PRODUCTION

(I) Macro@iytes Fleshy algae are not often a conspicuous element on coral reefs and tropical shores

(Johnston, 1969; Dahl, 1974). It would seem that for this reason there has been little work done on their role as primary producers. According to Dahl (1974) and Doty

20 BRB 52

J. B. LEWIS

Table 2. Primary production values for pelagic, benthic and terrestrial ecosystems

Habitat Pelagic

Marine North Sea English Channel Long Island Sound Sargasso Sea (Oligotrophic) Peru Current (Eutrophic)

Oligotrophic lakes Eutrophic lakes Sewage treatment ponds,

Benthic, littoral, and shallow water

Freshwater

California

Marine Algal beds, Nova Scotia Algal community, Canary Isles, Kelp Community, Nova Scotia Tropical marine grass beds

Coral reef

Estuarine and brackish water Spartina marsh, Georgia

Terrestrial Field grass, Minnesota

Sugar cane, Java Woodland deciduous

Birch Alder

Woodland coniferous

Biomass (gC/m8)

3 ‘5

8 0.87

I 4

2

- - 24

I 600 630 265

2260

196

280 - -

- 840 43 5

740 640

1700

I 760 3400 I 840

I 0 0

I35 470 134

3650

7-25 75-50

I 800

920

1750 3836

4650

2100

4200 2900 I 320

520 I 600 430

500 140

3450

425 785 800

Author

Steele (1956) Harvey (1950) Riley (1956) Menzel & Ryther (1961) Menzel et al. (1971)

h n d (1970) Lund (1970) Goulake et al. (1960)

MacFarlane (1952) Johnston (1969) Mann (1972) Odum H. T. (1956), Burkholder et al. (1959)

Qasim & Bhattashiri ( I ~ I ) , Moore et al. (1968)

Odum & Odum (1955) Kohn & Helfrich (1957) Odum, E. P. (1967) Smalley (I 960) After Westlake (1963) McFadyen (1964)

Golley ( I 960) Bray et al. (1959) Giltay (I 898)

Ovington & Madgewick (1959) Ovington (1956) Ovington (1957)

Source: Crisp (1975).

(1974), they play a variety of significant roles in the reef ecosystem and the importance of fleshy algae as primary producers has not been recognized.

Hillis-Colinvaw (1974) investigated the rates of production of a number of calcareous green algae which are often common on reefs and are important as contributors to reef sediments. In dense stands of Halimda opuntia gross primary production was 1460 gC/m2/yr and net production 839 gC/m2/yr. Corresponding rates for Penicillus capitatus were similar.

Production rates of a number of macrophytes were also determined by Qasim, Bhattashiri & Reddy (1972) who found that rates of four species, Ulva lactuca,

Organic production on coral reefs 313 Cladophora fackularis, Hypnea cervicornis and Halimeda hemprichii ranged between 365 and 800 gC[m2/yr net. Production rates by algal communities from the Canaries reported by Johnston (1969) ranged between about 365 and 3650 gC/m2/yr net production. In agreement with other workers (Goreau, 1963 ; Drew & Larkum, 1967) he found that production rates of several species of green algae were considerably lower than those of brown algae.

Wanders (1976a) examined the distribution of benthic algae on a shallow coral reef in Curagao and measured production rates in enclosed vessels. He reported that in areas dominated by fleshy and filamentous algae gross production was 712 gC/m2[yr and net production 452 gC/m2[yr. The yearly gross primary production over the reef as a whole was 5650 gC/m2 while the net production was 2330 gC/m2/yr.

Wanders (1976b) has also investigated the production of the large brown alga, Slugassum platycarpum, in deeper waters on a reef at Curagao. Using light and dark bottle techniques he found that the plant community of Sargassum beds contributed 3840 gC/m2/yr gross and 2550 gC/m2/yr net production to the reef. These figures were similar to the values for production on a shallow reef.

Thus the values for gross production of macrophytic algae reported by various authors fit well within the range for coral reefs presented in Table I. In circumstances where there is a luxuriant growth, macrophytic algae make an important contribution to reef primary production.

( 2 ) Calcareous algae Calcareous red algae of the family Corallinaceae are prominent on rocky substrates

of reefs and tropical intertidal areas. These calcareous plants are responsible for the well-known algal ridge of Pacific reefs but are also abundant upon Atlantic reefs. Another family, the Melobesioideae, are common as encrusting forms on fleshy macrophytes and marine grasses (Humm, 1964).

In spite of their ubiquitous occurrence on reefs, their biological contribution as primary producers has been little studied. Sargent & Austin (1954) found that oxygen production by calcareous algae fell within the range of corals, based on wet weights of the specimens. The primary production of reef-building algae from Eniwetok Atoll was investigated by Marsh (I970), who found that the production of calcareous algae at the surface of the reef was of the same order of magnitude as those of other benthic producers. Gross primary production was approximately 550 gC/m2/yr and net production 240 gC/m2[yr. Marsh concluded that the reef-building activities of calcareous algae were more important than their role as primary producers.

Goreau (1963) calculated the rate of fixation of carbon during photosynthesis of a series of calcareous algae. Rates of photosynthesis were lowered by shading. Mean rates of carbon fixation in Chlorophyta were in the range of 6 to 50 ,ugC/mgN/h and in the Rhodophyta 20 to 90 ,ugC/mgN/h with the exception of lithothamnoids which all had rates of less than s,ugC/mgN/h. Because Goreau’s estimates were based on single specimens and in terms of nitrogen content, it is impossible to compare his results with those of Marsh (1970) or Hillis-Collinvaux (1974). Goreau, however, concluded that rates of carbon fixation by the Chlorophyta were in the same range as those of reef corals and about one-third to one-half of the rates of Rhodophyta.

20-2

314 J. B. LEWIS Littler (1971) and Littler & Doty (1975) regarded lithothamnoids as an important

component of the seaward edge of tropical Pacific reefs (41 yo coverage by Porolithon onkodes on the seaward slope). Net productivities of two species of crustose corallines (803 gC/m2 of thalluslyr for Porolithon onkodes and 876 gC/m2 of thalluslyr for Porolithon gardineri) were within the range of other reef primary producers but only contributed between 73 and 182 gC/m2 to the reef per year.

The measurements by Wanders ( 1 9 7 6 ~ ) of primary production of coralline algae also emphasize the importance of these crustose forms. He reported production values of 890 gC/m2/yr gross and 370 gC/m2/yr net.

Sournia (1976) published values of 1387 gC/m2/yr gross production in a community dominated by the coralline algae Neogoniolithon frutescens or about half of the gross production of 2628 gC/m2/yr for the reef community as a whole. From these and other published results of production by coralline algae it appears that these organisms are important contributors to reef production but their rates of production are somewhat lower than those for reefs as a whole.

(3) Boring filamentous algae Filamentous algae of the Siphonales group were considered by Odum & Odum

(1955) to be important primary producers. This was based on the discovery that these plants form a thick green band or layer in the surface skeleton of hermatypes and have a biomass some sixteen times that of the zooxanthellae. Halldal (1968), however, found that only a small (0.001) percentage of the incident light falling on coral colonies was able to penetrate to the filamentous green layer. Shibata & Haxo (1969) also found low light intensities penetrating the green layer. Kanwisher & Wainwright (1967) concluded that filamentous algae contributed very little to reef productivity in Florida. Thus, although photosynthesis does occur at very low light levels, it would appear from data on light absorption that algae boring into corals do not supply any substantial amount of primary production to the reef system.

(4) Marine grasses Marine grasses such as Thalassia testudinum are often associated with coral reefs.

Growth of these plants helps to stabilize shifting sediments (Ginsburg & Lowenstam, 1958) and creates habitats for other benthic organisms (Stephens, 1966). In addition, detritus produced from Thalassia testudinum is probably important for production of higher trophic levels (Fenchel, 1970). For these reasons considerable attention has been given to studies of primary production of Thalasia testudinum and it would appear that marine grass communities are highly productive and that this species ranks among the most productive of all plants (Odum, 1956; Westlake, 1963).

One of the earliest studies of Thalmsia testudinum beds in Florida (Odum, 1957) revealed that gross primary production reached as high as 3880 gC/m2/yr. In Puerto Rico production was lower (Odum et aZ., 1959) with gross values of 980 and 1350 gC/m2/yr in two locations. Under experimental conditions Qasim et al. (1972) again found high values for Thalassia testudinum production. They recorded an average gross production rate of 1401 gC/m2/yr. A somewhat higher figure has been noted by

Organic production on coral reefs 3'5 McRoy (1974) who considered 1500 gC/m2/yr net an average value for both tropical and temperate sea grasses.

A number of workers have calculated production of Thalmsia by direct measurement of increments of blade growth. Thus Greenway (1974) found an average annual dry matter production of 2165 g/m2 in Jamaica while Buesa (1974) reported a mean dry leaf production of 1800g/m2/yr in Cuba. By converting these values to carbon equivalents, the Jamaican and Cuban net production values are approximately 704 gC/m2/yr and 585 gC/m2/yr respectively. Similarly, Patriquin (1973) obtained mean values of approximately 368 gC/m2/yr in leaf production with renewal of blades every two weeks. In estimating rates of turnover for Thalassia, Zieman (1968) found between 4-5 and 6 g dry wt/m2/day of new leaf material or approximately 534 gC/m2/yr to 712 gC/m2/yr.These figures were based on new leaf blades produced every14-16 days. Burkholder, Burkholder & Rivero (1959) reported a biomass value of 5-66 kg dry wt/m2 of Thalassia in Puerto Rico and Westlake (1963) has calculated from this figure a community organic production of approximately 16 m. t/ha or 800 gC/m2/yr.

Production values for Thalussia communities thus vary between about 400 and 4000 gC/m2/yr and are within the range noted in Table I for reef communities as a whole.

( 5 ) Phytoplankton The consensus of opinion regarding the importance of phytoplankton as primary

producers in waters flowing over coral reefs is that it contributes very little to community production of the reef. Sargent & Austin (1949) showed that the production of phytoplankton was insignificant over a reef in the Pacific. Sorokin (1974) found that phytoplankton production in several reef localities was only about I I gC/mz/yr Sournia & Ricard (1976) obtained values of 1.4 to 9-8 gC/m2/yr from phytoplankton in a shallow lagoon in French Polynesia, and 37-5 to 153 gC/m2/yr in a deeper lagoon subject to fertilization from the land. Milliman (1969) found very low values for phytoplankton productivity over reef flats in the Caribbean and concluded that planktonic forms made no contribution to overall productivity.

Qasim et al. (1972) found the production values for phytoplankton in an atoll in the Indian Ocean were only slightly higher than those for the surrounding sea. On the other hand, Gordon, Fournier & Krasnic (1971) found values as high as 293 gC/m2/yr in a lagoon at Fanning Island in the Pacific. Nevertheless, most values are low when compared with production by the whole community (cf. Table I). For example, in discussing the production of a shallow reef at Curaqao, Wanders (1976~) noted that it had a gross production of 50-100 times the average gross production of the phytoplankton of the nearby Caribbean Sea. It appears that production figures for phytoplankton over reefs are about the same, except in special cases, as those for oceanic phytoplankton in the surrounding waters.

(6) Zooxanthellue The functional relationship between reef-building corals and their zooxanthellae is

still a controversial one. There have been a number of comprehensive reviews of the subject since the early studies of Yonge (1930) including Yonge (1963a), Smith,

316 J. B. LEWIS Muscatine & Lewis (1969)~ Stoddart (1969), and Muscatine (1973). The consensus of opinion is that the zooxanthellae interact with their hosts by translocating organic carbon to the host, affect the cycling of nutrients and regulate the calcium deposition by reef corals. Each one of these functions has a bearing on the processes of reef production.

Early studies of production of corals were in terms of oxygen production. Mayer (1918) noted that, if corals were kept in sunlight, the water became supersaturated with oxygen owing to the photosynthetic activity of the zooxanthellae. Verwey (1930, 193 I ) determined the amount of oxygen exchange of Acropora hebes in light and in darkness and found that the production of oxygen by zooxanthellae was 2.5 to 5 times greater than its consumption by both coral and zooxanthellae. Yonge, Yonge & Nicholls (1932) also found the oxygen production by zooxanthellae to be between 2 and 3 times more than the total oxygen consumption by coral and zooxanthellae, and that there was a diurnal cycle of oxygen production; the highest rates of oxygen production occurred before and at midday, and the rate diminished with depth.

Kanwisher & Wainwright (1967) measured rates of oxygen production and consumption in Atlantic reef corals at different light intensities using a recording polarographic electrode. They found a diurnal cycle of oxygen production and determined the minimum light intensities for photosynthesis for different species. Maximum ratios of photosynthesis to respiration varied from 1-9 to 5.8. Roffman (1968) measured oxygen production and consumption in Pacific corals with a polarographic electrode and found ratios of production to consumption of between 2 and 5. Franzisket (1969) used chemical methods to determine production to consumption ratios of between 2.9 to 3.4 in Pacific corals. This latter study also showed that there was an optimum light intensity for photosynthesis which was lower than the daily observed maximum.

Beyers (1966) made diurnal measurements of the carbon-dioxide metabolism of Porites furcata and found that maximum metabolism occurred in the morning. He also determined that ratios of oxygen production to respiration varied between 1-33 and 2.81.

Drew (1973) made in situ measurements of photosynthesis and respiration in corals in the Red Sea and off Jamaica, using the oxygen method and 14C fixation. He found that respiration was about one-third of gross production in a Goniastrea species.

Thus, in all the experiments reported, it has been shown that the amount of oxygen produced by zooxanthellae is equal to, or greater than, the respiratory requirements of the corals. But it is questionable whether any of this oxygen is needed by the corals in waters which are always saturated with oxygen (Yonge, 1972).

Of greater importance for comparative purposes is the rate of carbon production by corals. Kanwisher & Wainwright (1967) converted oxygen production to the weight of carbon fixed, and obtained values between 2.7 and 10.2 gC/m2 coral surface/day, or 985-3723 gC/m2/yr. These values are similar to those obtained for reef-community production (cf. Table I). Drew (1973) found between 4.8 and 17-9 pgC/g tissuelh but the results unfortunately cannot be compared with those of Kanwisher & Wainwright (1967) because they were expressed on a different basis. This is one of the difficulties in comparing the results of various authors. Rates have been expressed in terms of tissue wt, corallum wt, and most recentIy by Johannes & Tepley (1974) in terms of

Organic production on coral reefs 317 tissue area. The most useful method is probably that used by Kanwisher &Wainwright (1967), namely g/ma of coral surface/day.

Undoubtedly the zooxanthellae play a major role in coral growth and reef building by causing accelerated calcification in light (Goreau & Goreau, 1959,1960a, b; Goreau 1959~) . Photosynthesis appears to produce substances which are translocated to calcification sites and stimulate deposition (Pearse & Muscatine, I 971 ; Vandermeulen, Davis & Muscatine, 1972; Barnes & Taylor, 1973). Goreau (1959~) proposed that zooxanthellae enhanced precipitation of calcium carbonate by removing carbon dioxide from the calcifying milieu during photosynthesis. Simkiss (1964a, b) suggested that zooxanthellae can take up organic and inorganic phosphates which act as crystal poisons and interfere with aragonite formation. Pearse & Muscatine (1971) and Vandermeulen & Muscatine (1974) suggest that the zooxanthellae supply material needed for the organic matrix of the skeleton. Crossland & Barnes (1974) have proposed that excreted ammonia neutralizes protons during carbonate precipitation and thus stimulates calcification. Thus, while several hypotheses have been put forth, the biological mechanism of calcium carbonate movement in corals is still unknown, as is the quantitative utilization of the photosynthetic products of the zooxanthellae in skeleton formation. I t would appear from the work of Chalker (1976) that calcium transport in corals is an energy-consuming process.

The fate of the carbon fixed photosynthetically has been considered in a review by Muscatine (1973). There is ample evidence that there is translocation of algal products as proteins, carbohydrates and lipids to the coral tissue. An attempt to quantify the amount of carbon fixed by photosynthesis and passed to the coral tissue was made by Goreau (1961) who considered that it could supply only a fraction of the nutritional requirements of the coral. Von Holt & von Holt (1968) found that 40% of the total 14C fixed by photosynthesis was recovered from tissue of the coral Scolymia lacma. Similarly, 3650% of the total 14C fixed was recovered from the animal tissue in Pocillopora damicomis by Muscatine & Cernichiari (1969). Thus, although a substantial proportion of carbon fixed by the zooxanthellae appears to be translocated to the animal tissue it is not known whether this amount is significant in terms of the nutritional requirements of the coral. Details of the total energy requirements of corals are required before this question can be answered.

Finally, it has been proposed that the zooxanthellae may favourably influence the metabolism of reef corals by preventing the accumulation of toxic wastes (Yonge, 1940) or conserving and recycling animal wastes in a nutrient-poor environment (Muscatine, 1973).

V. NUTRIENT FLUX

(I) Phosphorus The importance of phosphates for plankton production in the waters of the Great

Barrier Reef region was considered by Orr (1933) and by Yonge (1940). Although phosphate concentrations were uniformly low, averaging 5 mg/m3, both authors emphasized the continuous renewal of nutrient salts. Phosphates are, however, of extreme importance for reef production because of their involvement in calcification

318 J. B. LEWIS and in coral growth. Johannes, Coles & Kuenzel(1970) and Pomeroy, Pilson & Wiebe (I 974) regarded phosphorus as being important for both zooxanthella production and coral growth, and suggested that corals may obtain their phosphorus from the zooplankton. Yonge & Nicholls (193 I) found that corals in a healthy condition removed phosphorus from sea water but that, under unfavourable conditions, their excretion of phosphate increased.

Concentrations of organic phosphorus were measured by Pilson & Betzer (1973) at Eniwetok Atoll before and after water had passed over the reef. Concentrations were low (mean value of 0.154 pg-atom/l and remarkably constant. There was no detectable change in phosphorus between upstream and downstream stations, nor did the phosphate concentration vary with the photosynthetic or respiratory activities on the reef. Only on an algal-covered area was there any change in phosphorus content. Pomeroy & Kuenzler (1969) showed that corals excrete phosphorus only slowly.

Odum & Odum (1955) also found low levels of phosphorus on the same reef at Eniwetok (0.32 pg-atomll). Gilmartin (1960) reported concentrations of phosphate at Eniwetok with an overall mean of 0.347 pg-atom/l and found values consistently higher in bottom water than in surface waters. These results were extended by Pomeroy et al. (1974) who found that there was a continuous turn-over of phosphorus in reef components. The water over surfaces dominated by a blue-green alga, Schizo- thrix, showed active uptake of phosphate in the light and a continuous loss at night. Two species of coral of the genera Acropma and Heliopora showed no net uptake or loss while a hydrocoralline of the genus Millepora showed continuous uptake. I t was concluded that the growth of reefs was not limited by the low phosphorus concentration because they have evolved either internal biochemical or external food-chain recycling loops to satisfy their needs for phosphorus. Johannes et al. (1972) were also unable to find detectable changes in phosphorus across the same reef and suggested that a recycling mechanism was present. However, Johannes & Gerber (1974) found that there was a net import of phosphorus to the reef from plankton and detritus.

Di Salvo (1974) emphasized the role that bacteria play in recycling phosphorus in reef communities and considered that ‘pools’ of dissolved phosphorus existed in spaces within dead corals. Patriquin (1972) found that while a proportion of the phosphorus needed for growth in Thalasia testudinum was derived from sediments, the sediments still stored phosphates. McRoy & Barsdate (1970) also suggested that stands of sea grasses may act as reservoirs of dissolved phosphate in estuarine waters.

The general conclusion from all these studies appears to be that while various forms of phosphorus may be in low concentrations they are renewed continuously and recycled within the reef system.

(2) Nitrogen As with phosphorus, nitrogen has been regarded as being conserved on reefs and

atolls (Yonge, 1972). Kawaguti (1953) found that reef corals can take up ammonia from the surrounding sea water in the light but release it in the dark. In a study of nitrogen excretion by Atlantic reef corals, Sloterdijk (1975) found that Mad~ucis

Organic production on coral reefs 319 mZi&l&, Porites porites and Favia fragum were ammoniotelic and excreted 68%, 71 yo and 48 yo respectively of their nitrogen as ammonia. In the dark these species excreted more than 10 times as much ammonia nitrogen as in the light, while corals that had lost their zooxanthellae excreted ammonia nitrogen at the same rate in both light and dark. Nitrogen, in the form of ammonia, was also taken up from the surrounding sea water at rates proportional to its concentration. This suggests that ammonia is there- fore removed by the zooxanthellae and they use it as a source of nitrogen.

Stephens (1962) found that corals can absorb organic nitrogen and Franzisket (1973, 1974) observed that corals took up nitrate from sea water under experimental conditions. This uptake was independent of light. Franzisket (1974) also found uptake of nitrates by the green alga Ulua Zactuca.

Nitrogen is available to corals and other reef organisms both in the form of organic nitrogen from plankton and detritus and as nitrate, nitrite, ammonia and dissolved organic nitrogen. However, to judge from all accounts, the amount of nitrogen available in all forms is extemely limited. While Yonge (1972) has pointed out that nitrogen is utilized by reef corals, the work of Johannes et al. (1972) and Wiebe, Johannes & Webb (1975) is of particular interest. At Eniwetok Atoll, Johannes et al. (1972) observed that ocean water became enriched with various forms of nitrogen, both dissolved and particulate, as it flowed across a shallow reef. The net rate of nitrogen export from the reef was of the order of 3 kg/ha/day. The source of at least part of this nitrogen was found by Wiebe et al. (1975) to be nitrogen fixation by the blue-green alga, Calothrix crustacea, which fixed atmospheric nitrogen at the rate of 657 kgN/ha/yr. Such rates are amongst the highest reported for terrestrial or marine communities (Goering & Parker, 1972).

The observations of Patriquin (1972) on the marine grass Thalassia testudinum are of particular interest. He found that a significant proportion of the phosphorus and virtually all the nitrogen required for leaf growth were taken up from the sediments. Because regeneration of nutrients from organic matter in the sediments and from the sedimentlwater interface was insufficient to account for the nitrogen required, it appears likely that the nitrogen in the sediments is derived from the fixation of gaseous nitrogen by anaerobic bacteria. Support for this view was also obtained by Patriquin & Knowles (1972) who detected nitrogen fixation in the reducing substrate of the Thalassia testudinum root layer. Patriquin & Knowles (1972) estimated nitrogen fixation to be of the order of 100-500 kgN/ha/yr in a typical stand of Thalassia testdinurn. However, McRoy, Goering & Chaney (1973) found that rates of nitrogen fixation in Thalassia were extremely low or undetectable. Their results did not support the generalization that the process of nitrogen fixation supplied the nitrogen required for the high productivity of sea grasses.

Nitrogen fixation by epiphytes on Thalassia testudinum was noticed by Goering & Parker (1972) who found rates of nitrogen production between 2-4 and 16-5 ,ugN/mg plant N/hr. These figures result in values, on an area basis, of the order of 1050 kgN/ha/yr in an average standing crop of 200 g dry wt/m2.

Odum & Odum (1955) attempted to quantify the nitrogen budget in water over the reef at Eniwetok. They considered that 263 gN/ma/yr were required by the

320 J. B. LEWIS primary producers on the reef. Only about 219 gN/m2/yr were available from inorganic nitrate and, to meet the deficit, organic nitrogen would also have to be utilized. However, a nitrogen to phosphorus ratio of about 2 indicated a low availability of nitrogen. There was no evidence of uptake of a large amount of organic matter and it appeared that recycling of nitrogen must occur.

Kinsey & Domm (1974) artificially fertilized the water on a reef of the Great Barrier Reef with urea and mono-ammonium phosphate. Evidence was obtained of an increase in photosynthesis and there was an indication of increase in the standing crops of primary producers. This experiment also indicated a retention of nutrients in an isolated reef pool. Over a 9-month period the test area was maintained as an autotrophic environment whereas before fertilization it had not been autotrophic.

Much more work on nitrogen flux within the reef community is needed but the prevailing opinion appears to be that the resources of nitrogen are tightly cycled or conserved, at least with the coral plantlanimal association. Nitrogen fixation may make an important contribution to the amount in surface waters and a number of organisms have been shown to take part in such fixation.

VI. DETRITUS

The quantitative significance of detritus as food for corals and other benthic organisms on the reef has not been evaluated. However, there is a good deal of evidence to indicate that suspended detritus is abundant in the water flowing over reefs.

Glynn (1973 b) found that the dry biomass of suspended matter passing over a reef in Puerto Rico exceeded the dry biomass of net plankton by an order of magnitude or more. Evidence from examination of Millipore filters, plankton- pigment concentrations and productivity measurements indicated that the suspended matter was primarily detritus. The flux of suspended matter amounted to between 20-40 g dry wt/m2/day and there was no evidence of depletion of detrital material within the water mass flowing over the reef.

Johannes & Gerber (1974) found a net increase of benthic algal detritus and faecal pellets over a reef community at Eniwetok. More than 50% of the total organic matter in the sampleswas composed of fragments of benthic algae, equivalent to amean daily net import of approximately 0.27 gC/m2.

Marshall (1965) and Gerber & Marshall (1974) observed the abundance of particulate organic material in the form of algal fragments, faecal pellets, coral mucus and aggregated organic matter over reefs and in lagoons. Johannes (1967) discussed the role of coral mucus in the mobilization of organic aggregates. He regarded these sources as being used by the pelagic community over the reef but there seems to be no reason to suppose that such detritus is not captured by other invertebrates including corals. Gerber & Marshall (1974) noted that 95 yo of the gut contents of copepods in the lagoon area of Eniwetok Atoll consisted of detrital material. McCloskey & Chesher (1971) observed corals feeding on fish faeces.

Qasim & Sankaranarayanan (1970) found that the concentration of particulate organic matter over a reef in the Laccadives amounted to 20 % of the gross production of the

Organic production on coral reefs 321 reef community and was much greater than in the surrounding sea. Gross primary production was 12.3 gC/m2/day and particulate carbon production 2.28 gC/m2/day. The particulate matter acts as a source of energy for benthic organisms and zooplankton and it was suggested that this material is recycled over the reef.

Reiswig (1972) found values of 73-9 mgC/m2 as particulate organic matter in the waterlreef boundary layer over reefs in Jamaican waters. Only a small proportion of this could be accounted for as discrete particulate material while the rest was probably colloidal in nature. This unresolvable fraction of organic matter, which represents a carbon source seven times that of the discrete particulate material in Jamaican waters, is utilized by sponges and possibly other suspension feeders (Reiswig, 1971).

Richman, Loya & Slobodkin (1975) calculated the average concentration of particulate matter in the forereef region at Eilat in the Red Sea to be 4-4 g/m3. Of this amount, 2% was contributed by coral mucus.

Sournia & Ricard (1976) also regarded particulate matter over reefs as an important food for zooplankton, fishes and other organisms and they found that, on two coral- reef areas of French Polynesia, particulate matter was more abundant than phytoplankton.

There are, then, a number of studies which show that on crossing a reef, oceanic water acquires detritus which is then available to filter feeders and suspension feeders on the reef, including the corals.

Atlantic reef corals have been recently shown by Lewis & Price (1975,1976) to behave as suspension feeders. By means of nets and strands of mucus they are able to capture a wide range of particulate material as well as capturing zooplankton with their tentacles. Thus, when the biomass of zooplankton is too low to support the nutritional needs of corals (Johannes, 1974; Porter, 1974), other sources of food may be available to them. While those species with long active tentacles obtain food by means of tentacle capture and by mucous filaments, species with short tentacles such as the Agariciidae appear to feed entirely by suspension feeding. Lewis (1976) has shown experimentally that Atlantic reef corals are able to clear the surrounding water of particulate material.

Some interest has been shown in the potential nutrient significance of the mucus which is produced in copious amounts by most reef corals. Johannes (1967) observed mucus released by corals and the subsequent formation of aggregates of mucus and entrapped particles. Marshall (I 972) found considerable quantities of zooxanthellae in mucus discharged from coral heads. Suspended mucous strings were examined by Coles & Strathmann (1973) and found to have significantly higher organic carbon and nitrogen contents than suspended particles in the surrounding water. Benson & Muscatine (1974) found that the mucus from a variety of corals contained wax esters and they also observed that reef fish fed on the coral mucus. This is apparently one route by which energy-rich products of coral metabolism are transferred to higher trophic levels.

322 J. B. LEWIS

VII. ZOOPLANKTON

Opinions differ on the adequacy of zooplankton in satisfying the food requirements of corals and other benthic invertebrates on reefs. Johannes (1970, 1974) has argued that the biomass of zooplankton over coral reefs is insufficient to supply the energy needs although it may be important as a source of essential nutrients. On this view reef corals are ‘ autotrophic’ and depend extensively upon energy supplied by their zooxanthellae. On the the other hand, Yonge (1930), Yonge & Nicholls (193 I), and Goreau, Goreau & Yonge (1971) support the view that corals, as specialized carnivores, are dependent upon zooplankton as a food source.

The early papers of Sargent & Austin (1949, 1954) indicated that the zooplankton biomass of surrounding waters at Rongelap in the Pacific was too small to support all the benthic invertebrates on the reef. Johannes et al. (1970) calculated that zooplankton on a Bermuda reef was not sufficiently abundant to support the energy needs of the corals present as indicated by their rates of respiration. Johannes & Tepley (1974) found that the zooplankton biomass present could supply only 20% of the daily requirements for respiration in the Pacific coral, Porites Zobata, and Porter (1974) estimated that during a two-hour feeding period at sunset the Atlantic coral, Monta- strea annulayis, could capture only between 0-2 yo and I I yo of the total daily food required for energy used in respiration.

Studies by Tranter & George (1972) and by Glynn (1973b) have also supported these views. The former measured the biomass of zooplankton around two atolls in the Indian Ocean and found that it was depleted in the water flowing across reefs by between 23% and 60%. This suggests that the reef communities were nourished by oceanic zooplankton. Their calculations showed, however, that the magnitude of this food supply was low compared with the rates of primary production of the reef community.

Glynn (19733) made quantitative estimates of zooplankton over a reef at Puerto Rico. He, too, found evidence of the depletion of zooplankton in the water flowing across the reef of the order of 60 %, but it should be noted that there was considerable variation in zooplankton biomass seasonally and daily. The mean gain of net plankton (90-98 o/o zooplankton) to the reef was 0.18 gC/m2/day or about 68 gC/m2/yr. This was equivalent to between 4% and 13 yo of community metabolism.

Thus although the supply of oceanic zooplankton appears to be inadequate to support reef secondary production, reefs undoubtedly produce their own zooplankton (Emery, 1968). Sale, McWilliam & Anderson (1976) found that there was a resident plankton community at Heron Island, Australia, which was more abundant and richer in species than the offshore community. They suggested that this plankton community was retained on the reef by local circulation or by behavioural responses and was a potential source of food for the sessile reef organisms.

This opposing view, that reef corals are not wholly ‘autotrophic’ in their nutrition, has been summarized by Goreau et al. (1971). They regard corals as specialized carnivores without structural modifications for an autotrophic existence depending primarily upon zooplankton for their food. The work of Coles (1969) supports this view.

Organic production on coral reefs 323 He found that reef corals were able to ingest more than sufficient numbers of brine shrimp to cover their energy expenditure in respiration with energy left for storage and growth. Furthermore, Goreau et al. (1971) considered that reef corals may act as unspecialized detritus feeders (i.e. suspension feeders, Lewis & Price, 1975) upon a wide range of organic matter or may even utilize dissolved or colloidal organic matter.

The general conclusions regarding the importance of zooplankton to support reef production indicate that while there is a substantial removal of plankton by benthic organisms, zooplankton biomass from oceanic water flowing over reefs is too low even to supply the daily energy requirements of the corals present. Additional food must be supplied by resident plankton and other external sources.

VIII. MICROBIAL PRODUCTION

It has been pointed out by Di Salvo (1973) and Sorokin (1973 c ) that there are very few quantitative data on the role of microbial populations in the production of coral reefs. One cannot conceive of such complex systems without micro-organisms func- tioning as organic decomposers, nitrogen fixers and in biogeochemical processes. Large bacterial populations have been found in the carbonate sediments of reefs and may be important in processes of solution and precipitation (Emery, Tracey & Ladd (1954). Large numbers of bacteria on reef surfaces were reported by Odum & Odum (1955) and bacteria have been implicated in the high respiration rates of coral communities noted by Sargent & Austin (1949). The recent work of Di Salvo (1969, 1971, 1972, 1973, 1974) and Di Salvo & Gunderson (1971) have been concerned with the diversity and abundance of bacteria on coral reefs while Sorokin (1971 a, b, 1973a, b, 1974) has emphasized the role of bacteria in secondary production in reef organisms, that is, transforming detritus to microbial biomass.

Di Salvo suggested (1969, 1971) that the finely divided sediments in reef spaces and cavities functioned as ‘regenerative surfaces’ and that the rapid rates of oxygen consumption occurring in these cavities indicated rapid organic decomposition. Plate counts of sediments at the bases of coral heads showed densities of 107-108 bacterialg dry matter and amongst them were forms capable of digesting chitin and other organic compounds. Di Salvo (1973) subsequently found bacteria capable of reducing nitrates and digesting gelatin and agar.

The bacteria in reef sediments and in internal cavities were considered to have a role in nutrient regeneration (Di Salvo, 1974). Pools of dissolved nitrogen and amino nitrogen were found in sediments and in dead coral heads. Quantitative estimates gave values of 33 pg-atoms of phosphorus and 30 pmoles of amino nitrogen/m2 on dead coral surfaces. His results show that bacteria may thus be important in cycling of nutrients in the reef system.

Sorokin (1973~) has also stressed that the biomass of bacteria in reef sediments is very high, up to 150 mgC/1 of the sediment. Material scraped from surfaces of dead corals produced between 50 and IOO mgC/1 of sediment scrapings. Upon considering the role of bacteria in the production processes of tropical water, Sorokin (1971b) found that their biomass in the surface layers of the tropical Pacific averaged

324 J. B. LEWIS 15-30 mg/m3 but this could increase IOO times in shallow coastal waters. The very high biomass of bacterioplankton in tropical waters led Sorokin (1973a, b) to recognize their importance in processes of mineralization and nutrient cycling on reefs and also to consider their importance as food for secondary consumers. Results of feeding experiments (Sorokin, 1 9 7 3 ~ ) showed that six species of reef corals could consume bacterioplankton. Other forms which were able to filter bacterioplankton from water were the tunicate Ascidia nigra, the sponge Toxadocea violacea, and the oyster Crassostrea gigas. Sorokin (1973 a) regarded the bacterioplankton as being a high-quality food adequate in amount to supply a large percentage of the total energy needs of suspension feeders on the reef. Sorokin (1974) also noted that sediment consumers such as holothurians consumed bacteria equal to as much as 10% of their body weight in their daily diet. His calculations indicated that the bacterial population is an important intermediate link in the trophic chain through which energy produced by primary producers and from detritus is passed into the biological production of coral reefs.

IX. SESSILE INVERTEBRATES OTHER THAN CORALS

The notion of great abundance and diversity of species on a coral reef also applies to sessile invertebrates other than corals. Grassle (1973) regarded the variety of fauna and flora as the most obvious characteristic of coral reefs. In spite of the tremendous range of invertebrate species other than corais, there is little information upon which we can base estimates of their importance in reef production. In the many descriptive studies of reefs and reef zonation (Manton, 1935; Wells, 1957; Goreau, 19593; Lewis, 1960; Stoddart, 1962; ROOS, 1964; Storr, 1964; Kissling, 1965; Mergner, 1971; Glynn, 1973 a; and others), a wide variety of invertebrates is included, but quantitative estimates of the fauna are usually lacking.

That the numbers of invertebrates associated with corals may be high has been shown by Grassle (1973) who found 1441 polychaetes belonging to 103 species from a single coral head weighing 4-7 kg. Other workers who have also been impressed by the density of coral-associated invertebrates include Taylor (1968, 1971), Taylor & Lewis (1970), McCloskey (1970), Hutchings (1974) and Thomassin (1974), but they have not provided data upon which figures for the production of biomass can be based. There is obviously a need for more data of this type.

Odum & Odum (1955) have quantified the biomass of all sessile organisms at Eniwetok and found that on some areas of a reef biomass of consumers other than corals may be equal to or greater than the biomass of live coral tissue. However, because of the method of measuring production over the reef it was not possible to determine individual rates of production of sessile forms.

Associated invertebrates certainly have an effect on coral growth and reef structure. Patton (1976) has reviewed the associates of reef corals and considered some of the interactions that exist between corals and their inhabitants. Bakus (1973) noted that holothurians rework sediments on reefs, often at substantial rates such as I kg dry weight of sediment passed/m2/yr for Holothwia dt@cilis. Kinzie (1970) found that gorgonids could modify the growth patterns of corals. Glynn (1973 c) found that the


Table 3. Numbers and biomass of associated invertebrates per m2 of Porites furcata reef

Group No. individuals Biomass (g dry wt)

Scleractinia Zooanthidae Po 1 y ch a e ta Sipunculida Crustacea Mollusca Echinodemata Pisces

Several colonies 2 colonies

23 160

2 668 I37

15

20

2 002

12 002.3

6.7 1'1

0.9 40'3 59'4 263 '3

6-1

Source: Glynn (1973 c).

zooanthid, Palythoa mammillosa, can overgrow and exclude corals and concluded that other competitive interactions occurred between corals and associated sessile invertebrates. He has compiled a list of preliminary data on biomass densities of the associated invertebrates on a Porites furcata reef. This is shown in Table 3 and indicates that although the number of individuals is large, biomass is low compared with that of the corals themselves.

X. FISH

Fish have been considered to play an important role in the reef economy, not only in the production of sediments but also as herbivores and predators. Probably the most direct effect of fish on coral-reef production is predation on the corals themselves. Randall (1974) has recently reviewed the subject. The commonest fish feeding directly on coral polyps were the plectognaths - mainly trigger fish (Balistidae), file fish (Mono- canthidae), puffers (Tetraodontidae), and the butterfly fish (Chaetodontidae). In the West Indies, Randall (1967) found that predation on corals was limited to ten species and that coral fragments comprised only a small portion of the total food ingested. Randall (1974) regarded the abundance of fish that feed directly on coral as being low, not only in the number of individuals but also the number of species. Nevertheless he noted that corals damaged by grazing fish were likely to be killed by the invasion of algae and other secondary colonizers which weaken the skeletons.

On the other hand, Hiatt & Strasburg (1960) found considerable utilization of corals by parrot fish (Scaridae) in the Marshall Islands. Scarids were also regarded as feeding on coral occasionally by Goldman & Talbot (1976) in a review of the ecology of coral reef fishes.

Apparently much more important in the economy of reefs is the habit of many reef fish of grazing on the algae of hard surfaces (Hiatt & Strasburg, 1960; Randall, 1967). Rates of reef erosion by grazing fishes have been estimated by Cloud (1959) to produce between 420-615 metric tons/km2/yr of fine sand and by Bardach (1961) 200-300 tons/km2/yr, equivalent to a deposition rate of 1-3 mmlyr.

The production of fish on reefs has been considered by a number of authors primarily in relation to their potential as fisheries. As a result many of the smaller forms

326 J. B. LEWIS

Table 4. Estimates of abundance of f;Fh on nutural and arti3cial reds

Location Net weight

( d m 3 Authors

Offshore reef, Great Barrier Reef 209 Talbot & Goldman (1972) Fringing reef, Hawaii 62 Brock (1954) Reef flat, Eniwetok Atoll 9 Odum & Odum (1955) Patch reef, Bermuda 49 Bardach (1959) Fringing reef, Virgin Islands I 60 Randall (I 963) Fringing reef, Virgin Islands 38 Dammann (1969) Artificial reef, Virgin Islands 1750 Randall (1963)

Source: Stevenson & Marshall (1974).

such as Chaetodontidae have been underestimated. Population estimates have been mainly derived from census counts underwater or by rotenone poisoning.

Comparisons of biomass of fish on various reefs have been made by Stevenson & Marshall (1974) and are shown in Table 4. The largest numbers of fish are apparently found in outer reefs whereas lagoons and inner reefs support smaller populations.

The numbers of fish on reefs may be very high, as much as 5-15 times that on representative North Atlantic fishing grounds and twice the average of those in typical temperate lakes. Bardach (1959) has estimated the production of reef fishes at Bermuda at 2.2 x 105 kcal/ha/yr, while Goldman & Talbot (1976) in a review of the ecology of reef fishes have concluded that a maximum of 2000 kg/ha of fish could be maintained by reef communities.

Bakus (1967) computed the primary production on a reef flat at Eniwetok Atoll and related this to energy requirements of grazing parrot fish. He found that the net production of blue-green algae was about 2 g of organic matter/m2/day or I gC/m2/day. The total productivity of Cyanophyceae on the reef flat was roughly 520 x 103 kcal/day. The energy needed to support the estimated population of parrot fish within the same area was 22 x 103 kcal/day, leaving a surplus of 498 x 103 kcal/day for other grazers or to become detritus. Bakus (1966) also noted the lack of fleshy algae on many reefs and considered that the grazing habit of reef fish was partly responsible. Grazing may be heavy in some areas as indicated by Talbot (1965) who found that 20% by weight of the fish on a reef in East Africa are coral feeders.

While the quantitative significance of grazing and predation is not fully established, the grazing by herbivores and partial degradation of primary producers is one of the ways in which the plant biomass is made available to other trophic levels as detritus.

The importance of herbivory in this respect has been noted by Hiatt 8t Strasburg (1960), Bakus (1966), Randall (1967)~ and Goldman & Talbot (1976).

XI. TROPHIC RELATIONSHIPS

Coral reefs are so complex that, although much detailed work on individual components has been carried out, it has been difficult to synthesize them into a unified whole to define trophic relationships or to identify pathways of energy flow. The need for a trophic classification of reef systems has been proposed by Sournia & Ricard (1976).

Algae Algae in Algae in Seaweed shingle dead heads clumps in

coral -

327

100 200 300 400 500 600 700 1 1 I I I I I 1

Dry biomass (g/m2)

Fig. 3. Biomass pyramid of weights of living organisms from a coral reef at Eniwetok Atoll in the Pacific. Source: Odum & Odum 1955.

The most detailed study of trophic relationships has been that of Odum & Odum (1955) who constructed biomass pyramids of reef components at Eniwetok (Fig. 3) Ten different kinds of primary producers were accounted for with an average biomass of 703 g dry wt/m2. This included zooxanthellae and boring algae in the coral as well as fleshy macrophytes. The standing crop of herbivores was 132 and of carnivores 11 gIm2. Thus the biomass of herbivores was 18-9y0 of the biomass of primary producers, and that of the carnivores was 8.3% of the biomass of the herbivores. An annual turnover (ratio of annual primary production to average standing crop) of 12.5 times was computed. These calculations led to the conclusion that there was a rapid recycling of organic matter in the system. The fact that production as a whole on the reef was just about balanced by respiration suggested that the reef community was an ecological climax or open steady-state system.

Further consideration of Fig. 3 indicates that a substantial proportion of the biomass of consumers is composed of coral polyps. Odum & Odum (1955) have shown that between 15 and 60% of the reef surface is covered by living coral and other workers have estimated varying percentages of coral cover. Ott & Lewis (1972) found that up to 10% of the bottom surface on a fringing reef in Barbados was covered by Porites porites, 7 yo by Porites astreoides, and up to 7 o/o by Montastrea annularis. Ott (1975) later found that corals cover about 30% of the bottom of an offshore reef in Barbados and other benthos about 7%. Davies, Stoddart & Sigee (1971) found that as much as 80 yo of sample quadrats on a reef in the Maldives was covered by living coral colonies, while Scheer (1971) found up to 90% coverage by living corals at Fadiffolu Atoll in the Indian Ocean. Thus corals themselves appear to be the most important single component of the second trophic level in some areas.

A general scheme illustrating trophic relationships has been attempted by Sorokin (1973~) and is shown in Fig. 4. This study emphasizes the importance of micro- organisms and the process of decomposition. It also suggests a shortage of phytoplankton as primary producers in the reef ecosystem and hence the minor importance of the phytoplankton/zooplankton trophic relationship.

21 B R E 52

Phytoplankton

+ Dissolved organic Macrophytes - material

Fig. 5. Trophic relationships within a coral reef community, emphasizing the importance of detritus.

+ Bacteria Corals *

One is thus led to consider other possible trophic relationships. A number of reef studies have shown that water passing over a reef becomes enriched with detritus and this raises the possibility of a detritus-based food chain such as exists in mangrove swamps (Odum & Heald, 1975) Feeding strategies for particulate food sources other than zooplankton are different from strategies in which zooplankton is the main food

Benthos, fishes

Zooplankton b 4

Decompo- sers

Herbivores + -b Detritus

Organic production on coral regs 329 source (Jsrgensen, 1966). Filter feeding and suspension feeding are two ways of capturing particulate matter and Crisp (1975) has recently commented on the fact that suspension feeders require less energy for feeding than do zooplankton feeders. The proportion of suspension feeders (including corals) and filter feeders on reefs have been estimated by Glynn (1973 a ) who found that the total biomass of the macrobiota at Panama was 41 I g proteinlm2. Of this, 285.5 g consist of corals and 14.6 g of other suspension feeders. If, as Crisp (1975) suggests, suspension feeders are intrinsically efficient converters of energy then such a feeding strategy based on detritus is particu- larly suitable for zooplankton-poor tropical waters. With this view in mind an attempt to sketch trophic relationships within a coral reef community, incorporating detritus as a food source, is shown in Fig. 5.

XII. CORAL GROWTH

Investigations on the growth of reef corals has been directed towards two ends - estimation of the production of new coral biomass and of geologically meaningful rates of reef growth. Because of the complex nature of accumulation and erosion of coral in relation to total reef mass, the second objective cannot be directly derived from the first. From the point of view of estimating organic production of corals, studies of coral growth up to the present time have little value since the measurements have all been in terms of skeletal accretion. The relationship which the energetic requirements for tissue growth, metabolism and reproduction have to skeletal growth has not been evaluated. Thus it is not possible to relate coral growth, as it has been measured, to the rate of organic production on a reef. This is obviously a fruitful field for future work.

A comprehensive review of coral growth has been prepared by Buddemeier & Kinzie (1976) and in view of the foregoing remarks the subject need not be considered in detail. However, it is worth noting that Buddemeier & Kinzie have emphasized the variability of rates of coral growth, due to environmental variations, to inherent species variation and in large part to the methodology. Whether or not such variability occurs in tissue production of corals remains to be discovered but the need for careful measurements is underlined.

XIII. GROWTH A N D EROSION OF REEFS

(I) Carbonate production Though there is quite considerable literature on the subject of carbonate production

on coral reefs, this aspect of reef production lies beyond the frame of reference of this review and except for quantitative considerations will not be covered in detail. A useful review of the subject has been published by Chave, Smith & Roy (1972).

As was pointed out by Stoddart (1969), it is difficult to estimate the rates of reef accretion from data on coral colony growth. An actively growing reef is composed of organisms that produce and bind the hard structure as well as those which erode and destroy it. Rates of growth and erosion in terms of pathways or flow of calcium carbonate through the reef ecosystems have been published by Chave et al. (197z), Smith (1g73), and Macintyre, Smith & Zieman (1974). Table 5 shows estimates of

21-2

3 30 J. B. LEWIS

Table 5. Estimates of calcium carbonate production on coral reefs

Reef location

Fiji Eniwetok Rongelap Samoa Florida-Bahamas Florida Hawaii Fiji Eniwetok Bikini Cocos- Keeling Hawaii Fiji Pacific Jamaica Hawaii Bikini Bermuda Samoa

35 000 31 ooo 24 ooo 23 ooo

8 IOO

7 400 7 000 6 800 5 400 4 I00 3 000

22 000

2 200 2 000

I 600 I 400 I 400 I 400 I 400

26 16 14 9-24 6-25

5 '5 5'2 5 4 3

I .6 1'5

4-8

2

1'2 I

0.9-1 '3

8 I

Reference

Gardiner (1903~) Odum & Odum (1955) Sargent & Austin (I 949) Mayor (1924~) Vaughan (1915) Hoffmeister & Multer (1964) Easton (I 969) Gardiner (1903~) Chave et al. (1972) Emery et al. ( I 9 54) GUPPY (1859) Smith et al. (1970) Gardiner ( I 903 a) Dana (1872) Gorem & Land (1974) Oostdam (I 963) Emery et al. (1954) Schroeder & Ginsburg (1971) Mayor (1924~)

Source: Chave et al. (1972).

calcium-carbonate production from reefs in both the Atlantic and the Pacific. Chave et al. (1972) have attempted to distinguish between the various forms of production. They found that potential production, the amount of carbonate produced per unit area of reef surface covered by living organisms, was about 104g calcium carbonate/mZ/ yr. Gross production, the amount of carbonate produced by the reef community per unit area of sea floor, was 4 to 6 x 104 g of calcium carbonate/m2/yr and net production, the amount of carbonate retained by the reef system, was about 103g calcium carbonate/m2/yr.

In addition to skeletal deposition, calcium carbonate is also added to reefs in the form of sediments. I n terms of total carbonate production the unconsolidated sediments produced by reefs are more important than the structural skeletons themselves (Stoddart, 1969; Milliman, 1974). The ways in which such sediments are altered and cemented into the reef are discussed by Milliman (1974).

(2) Boring organisms The importance of boring organisms in corals was noted by Gardiner (1903b) and

Otter (1937). General reviews of this subject have been prepared by Otter (1937), Ginsburg (1957), Yonge (1963b) and Milliman (1974). A wide variety of organisms including sponges, sipunculid and polychaete worms, molluscs, crustacea and algae, are able to bore into corals. Burrowing is achieved by both mechanical and chemical means. Destruction of corals is caused not only by carbonate degradation and by borers but also by exposure of fresh surfaces to chemical dissolution and weakening of the skeleton. Rates of erosion of reef surfaces by borers are difficult to estimate but

Organic production on coral reefs 331 Neumann (1966) estimated that the sponge Clione lampa can excavate I to 1.4 cm/yr. Quantitative estimates of the volumes of coral skeletons removed and reworked by borers may vary from 3 to nearly 70% of the whole corallum (Hein & Risk, 1975; MacGeachy, 1975).

(3) Predators The recent increase of populations of the starfish, Acanthaster planci, on Pacific

reefs has focused interest upon predators of corals and on their potential for reef destruction. Robertson (1970) has reviewed the known predators of corals, all of which may assume local importance. They include polychaete worms (Marsden, 1962 ; Glynn, 1963), gastropods (Ott & Lewis, 1972), crustacea (Glynn, 1963), sea urchins (Bak & van Eys, 1975), and fish (Randall, 1967).

By far the most important coral predator is, of course, the starfish, Acanthaster planci. There is already an enormous literature on this subject and reviews of the subject have been prepared by Chesher (I970), Randall (1972) and Endean (1973,

(4) Pollution There has been much concern in recent years over the effect of pollution on coral

reefs. In a comprehensive treatise on tropical marine pollution edited by Wood & Johannes (1975), the sources and impact of pollution on reefs are reviewed. The editors have considered that the impact of pollutants and their rate of uptake increases with increasing temperatures, i.e., tropical communities have a low tolerance to pollution. Public concern over pollution on the Great Barrier Reef has been notable, and Endean (1976) has discussed and reviewed the effect of human activities on reef communities. It is apparent from these reviews that the various forms of marine pollution are having a harmful effect upon coral reefs everywhere.

Other important reviews of various aspects of pollution on reefs have been published by Johannes (1970, 1975), Smith, Chave & Kam (1973), and by Banner (1974).

'974, 1976).

XIV. HYDROGRAPHIC CONDITIONS

Differences in coral reef production and development are almost certainly related to local hydrography. Because of their proximity to land, fringing reefs can be influenced by coastal water run-off while atolls and barrier reefs are affected by oceanic conditions. Nevertheless, there have been few attempts to relate reef production to hydrographic conditions.

Maxwell & Swinchatt (1970) were able to correlate regions of prolific reef growth along the Queensland continental shelf with the nearness of a steep continental slope and considered that upwelling of deep water enhanced reef development. Orr (1933) also concluded that upwelling of nutrient-rich water contributed to reef production on the Great Barrier Reef. Brandon (1973) considered that only small-scale upwelling accrued along the outer Barrier Reef and that any nutrient-rich water would not penetrate the shelf or inner reefs for any appreciable distance.

Circulatory patterns in and around atoll reefs have been more closely examined than

332 J. B. LEWIS the currents influencing barrier and fringing reefs. The flow of water into Fanning Atoll and the circulation within the lagoon have been described by Gallagher et al. (1971) and are of interest because they demonstrate the conservation of water within a reef system. At high tide, oceanic water was driven into a lagoon as jets through channels and breaking waves drove water across the reef flat. Eddies developed within the lagoon and current jets of up to 3 knots were recorded. This ocean water was mixed with lagoon water through tidal inflow. About 70% of the water leaving the lagoon on an ebb tide entered on the previous flood while the remaining water was ' old lagoon water'. Since the tidal inflow and outflow over 24 h were about 10% of the lagoon volume, it took about a month for a complete exchange to be effected.

During slack tide there was an outflow in all directions but funnelled into the channels developing into jet-like flows on the seaward side. Thus the residence time of lagoon water was relatively long in Fanning Lagoon and replacement of water appears to be a slow process. The significance of this slow mixing is that any nutrient enrichment from oceanic water must be minimal but, as Gordon (1971) has pointed out, only a small percentage (0.4 yo) of the daily production of the lagoon is lost to the surrounding ocean by tidal exchange.

The studies at Fanning Atoll by Gallagher et al. (1971) and also by Guinther (1971), Gordon (1971), Gordon et al. (1971), and Smith (1974) thus illustrate the conservation of water within atoll lagoons. They also support the view that such conservation has a beneficial effect upon production. Gordon (1971) found a high rate of production in the lagoon and concluded that this was due to the low flushing rate. On the other hand, Kinsey & Domm (1974) showed that a lagoon at One Tree Island, Great Barrier Reef, was nutrient-limited and had a moderate rate of production.

The importance of hydrographic conditions for development of fringing reefs has been considered by Glynn & Stewart (1973) who concluded that upwelling of currents on the west sides of islands off the coast of Panama prevented coral growth. In the area studied, strong offshore winds from January through April produce a mass transport divergence which causes a lowering of sea level and consequent upwelling of relatively cold water rich in micronutrients. Mean primary production in inshore waters increases by a factor of two. In spite of this nutrient enrichment, however, the lowered temperatures (10 "C) inhibited coral growth.

Detailed studies by Glynn (1973 a, b) of the hydrography in and around a Caribbean fringing reef at Puerto Rico showed a rapid modification of the reef-flat habitat caused by exposure at low tides and by storms. At Puerto Rico the geostrophic surface currents move in a westerly direction during both winter and summer at velocities close to 1.5 km/h. The topography of the shoreline and insular shelf allow the inshore currents to follow a similar course and thus a continuous surface current flows past the coral reefs. For this reason the reef development is strongly influenced by conditions of wind and tide that control the flow of water over the reef.

As a consequence of seasonal variation of atmospheric and hydrographic conditions, Glynn (1973b) found that peak abundance of plankton was correlated with increasing wind speed and current velocity in the spring and with increased precipitation in the autumn. Plankton blooms in the autumn were perhaps initiated by nutrient

Organic production on coral reefs 333 enrichment due to fresh-water run-off and the effects of mixing during strong cyclonic disturbances. Since depletion of zooplankton was observed in water flowing over the reef, vigorous circulation of water would be expected to increase levels of secondary production.

The work of Glynn also brings into focus the results of other authors who have shown that extreme physical conditions have a great effect upon reef development. Thus Stoddart (1962, 1963, 1969) has shown the destructive effects of hurricanes to reefs in British Honduras while exposure at low tide has had catastrophic effects in Palao (Motoda, 1940), at Eilat (Loya, 1972), and in Jamaica (Jackson, 1972). Circula- tory systems have been shown to affect reef systems at Bermuda (Boden, 1952), in Florida (Jones, 1963), the Bahamas (Storr, 1964), and off Nicaragua (Milliman, 1969).

Waves are possibly just as important as currents in their effects on reef morphology. The spur and groove system, which is a common feature of many reefs, was found by Munk & Sargent (1954) to be related to the distribution of wave activity at Bikini. Roberts (1974) found that the formation of well-developed reef buttresses and steep profiles was associated with high wave energy coastlines in the Cayman Islands. Low relief and more gentle slopes were associated with low energy areas. Higher productivity in terms of biomass and uniformity of structure were also characteristic of high levels of physical stress and were missing from low energy areas. Roberts, Murray & Suhayda (1975) concluded that reef morphology responds to the synoptic distribution of wave power.

Thus, in a variety of ways, hydrographic conditions may have beneficial or harmful effects upon reef production. Conservation of water in enclosed lagoonal areas enhances production while excessive wave action and storms may cause massive destruction.

XV. DISCUSSION

Any discussion of production processes on coral reefs must inevitably be centred around consideration of the reasons for the high production rates attained by reef systems in comparison with other marine ecosystems. Recent comparisons of production rates have been provided by Crisp (1975), Dunbar (1975) and Rodin, Bazilevich & Rozov (1975), and their data confirm the view that coral reef production is as high as that of the most fertile marine waters.

The problem of how this production is achieved was first raised by Sargent & Austin (1949) who found that reefs developed high rates of primary production in nutrient-poor and relatively barren oceans. Their observations were later confirmed by other workers, and from all accounts rapid rates of production of algae and sea grasses are characteristic of the warm, shallow waters in which coral reefs flourish. A fundamental reason for the high primary production is, of course, the abundant light energy available. On the other hand, the low levels of nutrient elements such as nitrogen and phosphorus in the water flowing around and over reefs would appear to impose limits on primary production.

While nitrogen has been regarded as being limiting €or plant growth on reefs, recent work by Johannes et al. (1972) has, in fact, shown that an excess of dissolved

334 J. B. LEWIS and particulate nitrogen is produced on reefs and exported to surrounding waters. The most likely cause of this is the ability of a number of primary producers to fix atmospheric nitrogen dissolved in the water. Nitrogen is fixed in the root layer of the sea grass Thalassia testudinum and nitrogen fixation occurs in some blue-green algae which form thick layers over rock surfaces on reefs. Epiphytic algae on Thalassia testudinum are also nitrogen fixers and Di Salvo (1973) has argued for the importance of bacteria as nitrogen fixers on reefs. While much more work needs to be done on the nitrogen budget of reef ecosystems it would appear that nitrogen is not, after all, a limiting nutrient but is fixed in substantial quantities.

The situation with regard to phosphorus is less clear. From all accounts the levels of phosphorus in tropical water are uniformly low and no increase in phosphorus concentrations over reefs has been reported. The usual reason given to account for high rates of primary production in spite of the low phosphorus levels is that phosphorus is continuously recycled. It may be argued that water flowing over reefs has a very short residence time except in lagoons and phosphorus produced over the reef would be quickly carried off. The fact that the highest rates of production are often in lagoonal areas suggests that nutrients in fact may be cycled most effectively where the water has a longer residence time.

A consideration of the flow of water over the reef suggests that while phosphorus and other nutrients may be low in concentration, nevertheless there is a constant supply. Reports by Vollenweider (1968) and by Schindler, Lean & Fee (1975) emphasized that nutrient flux should be considered as a rate of inflow and uptake and not judged in terms of concentration. Lean (1973) found that phosphate was rapidly taken up by phytoplankton and bacteria and began to be excreted within minutes. Thus an extremely small phosphate pool may be rapidly used and continuously replenished by the biota.

Given that high rates of primary production are characteristic of coral reefs, the next question to answer is how this production is mobilized to support the higher trophic levels. Again, we find that this problem was raised by Sargent & Austin (1949) who found zooplankton numbers “grossly inadequate” to support the biomass of benthic invertebrates. And yet coral reefs, like tropical rain forests, accumulate a high biomass or standing crop (Farnworth & Golley, 1973). Reference to Table I makes it clear that on almost every reef studied, gross production by the community exceeds its respiration. There is thus no problem in accounting for energy input. The main question is, by what pathways is the energy channelled into reef building?

Several possible pathways exist for the supply of energy for secondary production. These include recycling of carbon within the reef system, translocation of nutrients within corals themselves (again, a recycling mechanism), production and decomposition of detritus from primary producers, and utilization of zooplankton from surrounding waters and from indigenous stocks of reef plankton.

Reference to the studies by Marshall (1968), Qasim & Sankaranarayanan (1970), McCloskey & Chesher (1971), Johannes et al. (1972), Glynn (1973 b), Sorokin (1973 c), Johannes & Gerber (1974), and Marshall, Durbin, Gerber & Telek (1975) lead to the conclusion that there are considerable concentrations of particulate matter over reefs.

Organic production on coral reefs 335 This suggests that the primary production is broken down into particles of detritus and these become a source of energy for benthic organisms. Plant production may be reduced in a number of ways: by fish (Cloud, 1959; Bardach, 1961), by sea urchins (Lewis, 1964) and by the turbulent flow of currents and wave action over reefs. Because of the irregularity of the surface of reefs, and the presence of cavities and holes it seems likely that much of this detrital material is trapped within the reef framework. Detritus from primary producers is not available to carnivores directly, however, and Di Salvo (1973) has commented on the availability of rich bacterial flora in reef sediments for decomposition of organic material. Sorokin (1974) also emphasized the importance of bacteria in mobilizing primary production for secondary producers while Marshall et al. (1975) have described processes whereby particulate material is concentrated and flocculated. There is thus good evidence to show that secondary production on a coral reef may be based largely upon the supply of detritus.

From the evidence available, the supply of zooplankton imported from surrounding waters and developed within the reef system is not large enough to supply the total nutritional needs of corals themselves. However, it is known that plankton populations are depleted in water flowing over reefs and it is evident that zooplankton is at least a partial food source for corals and presumably other planktivores.

With respect to translocation of nutrients from zooxanthellae to coral animal, the movement of material is clearly established. However, the quantitative importance of this process in supplying nutritional requirements to the coral still awaits definition. It should be noted, however, that this pathway applies only to organisms with zooxanthellae and does nothing to solve the food problem of other benthic filter feeders and suspension feeders.

The view that nutrients and organic matter are tightly recyled or conserved within reef systems is almost universal in the relevant literature. This view implies a retention of water over reef communities in spite of rapid water transport. Furthermore, although recycling of both nutrients and organic material may occur, an external source of energy is still required in order to allow reef growth. One cannot live by taking in one's own laundry! Energy losses within the reef system may be minimized by recycling mechanisms such as in coral/zooxanthellae symbioses but ultimately a source of external energy is necessary. The high rates of primary production in the reef system based partly on nitrogen fixation and abundant light, and the production of detritus mobilized for second and third trophic levels, appear at this stage of our knowledge to be the most prominent productive mechanisms.

XVI. SUMMARY

I . The first quantitative studies of production on coral reefs were those of Sargent & Austin who showed that productivity on reefs was considerably higher than in surrounding waters. This high production occurred in spite of nutrient limitation and low productivity of offshore waters. Their conclusions have since been confirmed by numerous other workers in both the Atlantic and the Pacific.

2. Primary production on reefs has been studied by flow respirometry, measuring

336 J. B. LEWIS changes in oxygen or carbon dioxide concentrations in water flowing over reefs. Production of benthic organisms has also been measured in situ by light and dark bottle methods and by radioactive tracer techniques. Production values obtained by the various methods are not identical but their use in combination is to be recommended.

3. Rates of gross primary production on reefs vary between 300-5000 gC/m2/yr. These rates are higher than general oceanic values and as high as those of the most productive marine communities. 4. Sources of primary production include fleshy macrophytes, calcareous algae,

filamentous algae on the coral skeletons or calcareous rock, marine grasses and the zooxanthellae within coral tissue. Production values from the various sources fall within the range of production of reefs as a whole.

5. Concentrations of nitrogen and phosphorus in waters flowing over reefs are consistently low. There is evidence to suggest that both these nutrients are recycled rapidly on the reef and that nitrogen is fixed by bacteria and primary producers.

6. In many instances the mass of detritus over coral reefs exceeds the biomass of zooplankton. While the quantitative significance of detritus as food for corals and other benthic organisms has not been evaluated, there is a growing body of evidence to show that this may be the key to understanding secondary production.

7. Opinions differ on the adequacy of zooplankton in satisfying the food requirements of corals and other benthic invertebrates on reefs. The weight of evidence suggests that while there is a removal of zoopIankton by benthic organisms, the total biomass carried over the reef is too small to support the energy needs of secondary production.

8. Bacteria are a potential source of energy for secondary production on reefs and are implicated in nitrogen fixation, decomposition and biogeochemical cycling.

9. There is an abundance of sessile invertebrates other than corals on reefs but there are few quantitative data on their importance in secondary production. 10. The biomass of fish on reefs may be very high but the quantitative significance

of grazing and predation is not fully established. I I . Studies on the growth of corals themselves have been based on measurements of

skeletal accretion. These methods do not lead directly to estimates of reef organic production. Growth rates of corals vary considerably between and within species. 12. Estimates of reef growth have been made from measurements of coral growth

and from the flux of calcium carbonate. There is less quantitative information on erosion caused by mechanical damage, by boring organisms and by human pollution.

13. Hydrographic factors influence growth and form of reefs and there is some evidence to show that production is enhanced by conservation of water in lagoonal areas.

XVII. ACKNOWLEDGEMENTS

This work was supported by a Grant-in-Aid of Research from the National Research Council of Canada. I am grateful to Professors M. J. Dunbar and K. H. Mann for their helpful comments on the manuscript.


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XIX. ADDENDUM

The Third International Symposium on Coral Reefs was held in Miami, Florida, from 23-27 May 1977. New information on many of the topics discussed in this review was forthcoming and the reader is referred to published proceedings.

Documents

PROCESSES OF ORGANIC PRODUCTION ON CORAL REEFS