Coral Reefs (1989) 7:161q67 Coral Reefs �9 Springer-Verlag 1989

Spherical growth in the Caribbean coral Siderastrea radians (Pallas) and its survival in disturbed habitats

John B. Lewis

Department of Biology, McGill University, Montreal, Quebec, Canada H3A 1 B1

Accepted 2 February 1988

Abstract. Siderastrea radians (Pallas) is a common West Indian reef coral that displays wide morphological varia- tion. The hypothesis that a spherical form of free living colonies of S. radians has advantages for survival was ex- amined in Barbados, Colonies were sampled f rom tide pools and from random quadrats at four reef flat sites subjected to strong wave action. Survival was found to be a positive function of colony size measured as living sur- face area and was correlated with stage of development toward a spherical shape. The combinat ion of spherical shape and larger size confer a selective advantage on free living colonies in disturbed habitats.

Introduction

The considerable morphological variat ion that exists within some species of corals has long confused taxono- mists and intrigued coral reef ecologists. Early natural- ists, such as Duerden (1904), Vaughan (1902), Verrill (1901) and Wood-Jones (1907) frequently remarked upon the variety of forms of both corallites and coralla. The late Sir Maurice Yonge, in a report on the West In- dian coral genus Siderastrea, wrote that the great success of corals as a group was due to their capability for wide modification in form, enabling them to adapt to life in a variety of environments (Yonge 1935).

Different growth forms within coral species may be genetic polymorphs or environmentally induced pheno- types (Stoddart 1984) and the topic is a mat ter of current interest and controversy (e.g. Foster 1977, 1979; Hilde- mann et al. 1977; Potts 1976, 1984). Jackson (1979) has examined the advantages of variability within a species as par t o f a general model of morphological strategies of sessile animals. Deductions of the importance of mor- phological variation in a species lead to testable hypoth- eses about relative advantages for survival.

Siderastrea radians (Pallas) is a common West Indian reef coral that is capable of wide morphological varia- tion. Remarkable, free living, spherical coralla (coral-

liths) caught the attention of Duerden (1904), Verrill (1901), Yonge (1935) and more recently at tracted the in- terest of Kissling (1973) in Florida. Free living and spherical morphs also occur in other species of corals (e.g. Pavona and Porites spp.) and have been described by Gill and Coates (1977), Glynn (1974), Pichon (1974) and by Scoffin et al. (1985).

Siderastrea radians is a hardy, ubiquitous coral that is most frequently seen as flattened or hemispherical colo- nies cemented firmly to a hard substrate. According to Kissling (1973), coralliths are most common on rubble beds of the inner zones of reefs, subjected to continuous wave action. It has been suggested that the spherical form is a consequence of frequent physical disturbance (Kiss- ling 1973; Yonge 1935) or the rolling movement due to fish predation or other bioturbat ion (Glynn 1974).

The purpose of this study is to test the hypothesis that sphericity is an advantage to the coral Siderastrea radians in a disturbed habitat. Sphericity may be a mechanical re- sponse to being moved about, but may also be regarded as a pattern of growth and a life history trait which has selective advantage for the coral by lowering mortality.

Materials and methods

Samples of Siderastrea radians were collected from reef fiats at four simi- lar localities in Barbados. Two of the sites, Bath and Martins Bay, are vn the exposed windward east coast of the island, while Needham's Point and St. Lawrence are on the less exposed south coast near Bridgetown. Substrates at all four sites were similar and consisted primarily of small living colonies and dead fragments of branching Porites spp. and growths of the sea-grasses Thalassia testudinum K6nig and Syringodium filiforme Kutzing. Water depths were less than a meter at high tide and inner areas were exposed at low water spring tides. The tidal fiat at Mar- tins Bay during low tide is shown in Fig. 1 and the substratum of the Nccdham's Point fiat is shown in Fig. 2. All four habitats were subjected to moderate to heavy wave action except at low tide and all are consid- ered to be "disturbed" habitats, similar to those described by Kissling (1973).

Colonies of Siderastrea radians of all sizes (including small recently settled colonies as well as fully rounded coralliths) were collected from within both randomly chosen and contiguous quadrats along line tran- sects, and from isolated tide pools. Substrates of the tide pools were bare

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Fig. 1. Tidal flat at Martins Bay on the east coast at low tide

Fig. 2, Substratum at Needham's Point showing seagrass and rubble composition

Fig. 3. X-radiograph of sectioned corallith of Siderastrea radians showing core and growth bands, x 1

Fig. 4. Developmental stages of coralliths of Siderastrea radians. See Table 1 for description, x 0.42

Table 1. Stages in the development of coralliths of Siderastrea radians (Pallas)

1. Few to dozens of polyps, flat, encrusting colony on coral branch or irregular hard fragment

2. Rounded encrusting colony covering tip of branch or fragment like a sheath

3. Rounded or elongate colony, completely covering branch or fragment core except for attachment at base

4. Corallith, colony free, elongate or otherwise irregular in shape 5. Corallith, spherical or subspherical

of coral fragments and seagrasses. Shapiro-Wilk tests and normal prob- ability plots of colony data sets were computed and showed no violations of the assumptions of normality. Determination of corallith weights, di- mensions and sphericity followed the methods of Glynn (1974). Spheric- ity is defined as the cube root of LSI/L 3, where L, S and I are the long, short and intermediate dimensions, respectively. The surface areas of colonies were determined by wrapping the branches with aluminium foil and calculating coverage by measurements with an electronic planimeter and from known weight/area relationships according to the method of Johannes and Tepley (1974). Corallith ages were determined in full years by counting the number of light and dark pair bands oi1 x-radiographs of sectioned colonies (Fig. 3) according to the method of Scoffin et al. (1985).

Results

Over the size range of colonies of all sizes sampled, an as- sortment of shapes from flat encrusting colonies to large rounded coralliths could be discerned. These may be re- garded as stages in development of free living spherical coralla and can be classified, beginning with initial estab- lishment of juvenile colonies. Development stages are de- scribed in Table 1 and shown in Fig. 4. Initial settlement of planulae is upon fragments of assorted sizes and, as re-

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Fig.& Regression line showing strong positive relationships between mean corallith diameter and weight

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163

ported by Kissling (1973), continued growth leads to coverage of the fragment and a free living corallum with a central foreign core.

The range of sizes of coralliths was between about 25 and 70 mm mean diameter (average of short, intermedi- ate and long dimensions) and 15 to 300 g in dry weight. The largest corallith sampled had a mean diameter of 72 ram, weighed 297 g and was 4 years old. The range of sizes was similar to that obtained for massive coralliths of Pavona sp. and Porites sp. by Scoffin et al. (1985) at

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Fig.7. Scatter diagram showing lack of relationship between corallith sphericity and mean corallith diameter

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Fig. 6. Scatter diagram showing lack of relationship between corallith Fig. 8. Histogram (4- SE) showing increase in mean weight of coralliths sphericity and weight with age

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Rarotonga (Cook Islands) but somewhat smaller than those collected by Glynn (1974) in the Gulf of Panama.

As expected, there is a strong positive relationship be- tween mean corallith diameter and corallith weight (Fig. 5, r 2 = 0.98, n = 36) but no apparent relationship be- tween sphericity of the Coralliths and either weight or mean diameter (Figs. 6 and 7). Both weight and mean corallith diameter increased with age, as indicated in Figs. 8 and 9. Analysis of variance (Table 2) showed that means were significantly different between 1 and 2, 2 and 3, and 3 and 4 year old coralliths respectively. Figure 10 also shows an increase in sphericity of coralliths with age but analysis of variance (Table 2) of the data showed no significant differences between means. A regression of sphericity on age showed a weak but positive relationship (rZ=0.25, n--26, P<0.05). Thus, coralliths become larger with age but within the size range sampled, the trend towards sphericity is weak. Nevertheless, while the correlations between sphericity and age or size are not strong in coralliths, a trend towards sphericity, within the whole population, is evident in the sequence of develop- ment stages (Table 1 and Fig. 4).

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Fig. 9. His togram (4-SE) showing increase in mean corallith diameter with age

Table 2. A N O V A table from data for weight, mean diameter and sphericity variation of coralliths with age and of surface area with corallum development stage, ns = not significant; ** significant (P < 0.01)

Source of Degree of Mean F variation freedom square value

WT x age 3 22455 20.09** Residual 26 1 117 Diam x age 3 660 16.33"* Residual 24 40 Spher x age 3 0.02 2.97 ns Residual 24 0.01 Area x stage 4 7522908 74.94** Residual 203 100 382

An increase in surface area of coralla may be an esti- mate of growth, providing fragmentation or regression of colonies does not occur (Hughes 1984; Hughes and Con- nell 1987). There was an increase in mean surface area of living tissue with stage of development (Fig. 11) in colo- nies sampled in random quadrats. Analysis of variance (Table 2) showed that means were significantly different between pairs of stages from 1 to 5. Thus, both surface area and sphericity increase with the progression of de- velopmental stages which are age related.

If colony size and age are directly related (Figs. 9 and 11), then size-frequency distributions approximate sur- vivorship curves in which high juvenile mortality gives way to low mortality rates for older individuals (Hughes and Jackson 1980, 1985). From size-frequency distribu-

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Fig. 10. Histogram (__+SE) showing increase in sphericity of coralliths with age

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Fig. l l . His togram ( _ S E ) showing increase o f surface area of living coral with developmental stages of Siderastrea radians from colonies oc- curring in random quadrats

tions of the total quadrat samples at St. Lawrence and Bath (Fig. 12), it is apparent that the highest mortality oc- curs in the smaller colonies up to 10 cm 2 area and that large colonies are much rarer than small colonies. The mortality rate decreased between 10 and 35 cm 2 and is steady in larger colonies between 35 and 60 cm 2. The same relationships may be seen in Fig. 13 for the size-fre- quency distributions of encrusting colonies from eleven tide pools at Martins Bay. The highest mortality occurred

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Fig. 12. Size-frequency distributions of colonies of Siderastrea radians from 43 random quadrats at Bath and St. Lawrence, Barbados

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Fig. 13. Size-frequency distributions ofencrusting colonies of Siderastrea radians occurring in eleven tide pools at Martins Bay

165

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Fig. 14. Development stage-frequency distributions of Siderastrea radians per m 2 of substrate at Needham's Point and Bath

in colonies up to 10 cm 2 surface area. There was a de- crease in mortality in encrusting colonies between 10 and 25 cm 2 and the rate was steady in larger colonies between 30 and 65 cm 2 surface area. Thus, mortality decreases with increasing size as has been noted in other corals (Connell 1973; Hughes and Jackson 1985).

The same trend can be observed from the develop- ment stage frequency curves of Fig. 14, in which the number of coralla/m 2 are plotted against development stages. At two localities, Needham's Point and Bath, mortality rates decrease with advancing development stages. Thus, as coralla become larger and more rounded in shape, their mortality rates decrease. There is presum- ably an upper size limit attained by coralliths. Large, heavy coralliths are more likely to remain undisturbed and eventually lose their rounded shape (Laborel 1969; Glynn 1974).

Discuss ion

It has been argued from colony size-frequency distribu- tion data that mortality rates of S i d e r a s t r e a rad ians de- crease with increasing size, assuming size and age are di- rectly related. However, Hughes (1984), Hughes and Connell (1987), and Hughes and Jackson (1980, 1985) have cautioned against this assumption because partial mortality, fusion or fission in corals may distort the rela- tionship between size and age. Examples of this distor- tion appear in foliaceous and branching forms, in colo- nies of a few to many hundreds of cm 2 reef surface cover.

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In the case of Siderastrea radians we are dealing with colonies of much smaller size, f rom a few dozen polyps to tens of cm 2 live surface area. Connell (1973) and Hughes and Jackson (1985) found that mortali ty of corals was strongly dependent upon size and that mortal- ity rates declined sharply with increasing colony size. Small colonies are more susceptible to instantaneous or whole colony mortali ty than to partial mortali ty (Connell 1973). In the case of periodic disturbances they should es- cape or die completely (Hughes and Jackson 1980, 1985). Because of the detailed examination of individual colo- nies of S. radians for surface area measurements, the limits and contours of each colony were carefully noted. It was apparent that partial mortality, fusion and fission were uncommon and occurred in only 2 -3% of the small colonies examined, within stages I to 3. Neither fusion nor fission were observed in the larger coralliths of stages 4 and 5. Partial mortal i ty did occur in the spherical colo- nies but, because of the concentric growth of coralliths, was rapidly repaired and did not distort the sequence of banding throughout the colony as a whole (Scoffin et al. 1985). It appears then that S. radians is not as susceptible to partial mortali ty and fusion as are the foliaceous and branching species and therefore size-frequency distribu- tions are adequate descriptions of the populat ion struc- ture.

In Aeropora spp., survivorship of small fragment~ f rom storm damaged coral is also dependent upon size (Tunnicliffe 1981; Highsmith 1982). By all accounts, the mortali ty rates of very small fragments are high due to further breakage and abrasion, and so fragmentation will be selectively advantageous in those species of coral that break into pieces above a certain size range (Hughes 1983). Breakage and abrasion would be expected to in- crease with increasing intensity of physical disturbance. Survivorship is thus a positive function of colony size (Highsmith et al. 1980) in corals, whether the colony be a broken fragment or as in the case of Siderastrea radians derived f rom a settled larva.

In colonies of Siderastrea radians with living surface areas of 25 cm z and 26 cm 2 (Fig. 12) the percent mortali- ties were 89% and 9.6% respectively. Mortali ty rates of S. radians are thus higher than for corals reported by Connell (1973) who found 50% mortali ty in colonies with surface areas between 1 and 40 cm 2. The heavier mortali ty in the early stages of S. radians can be attrib- uted partly to the physically disturbed habitat.

The lack of significant positive correlations between sphericity and corallith weight or diameter in Siderastrea radians is consistent with the results of Glynn (1974) on Pavona sp. and Porites sp. coralliths of less than 100 g and can be explained by the irregular size and shapes of fragments which form the growth centres of the coral- liths. Scoffin et al. (1985) also found weak correlations between corallith weights and sphericity in Pavona and Porites spp. Thus, in S. radians as well as in Pavona and Porites spp., the shape of coralliths over the size range sampled is poorly predicted by weight or mean diameter.

Glynn (1974) observed that a sample biased to specimens heavier than 100 g showed a stronger correlation between weight and sphericity.

Highsmith (1982) concluded that fragment shapes most favorable for survival in damaged corals would be those well developed in three dimensions. Tunnicliffe (1981) found that Acropora cervicornis fragments with multiple branches were more likely to survive than un- branched fragments. In Siderastrea radians, the percent- age mortalities of growth stages 1 to 3, 4 and 5 were 80%, 13% and 6% respectively. Since both stages 4 and 5 are free living coralliths, mortali ty is lowest in those colonies with the highest sphericity, and coral mortali ty appears to be strongly shape dependent. An alternative explana- tion is that the decrease in mortali ty is due to increasing size only, as appears to be the case with the encrusting colonies of tide pools (Fig. 13) which attain a surface area of nearly 70 cm 2. Tide pools offer a microhabitat with a hard, stable substrate in contrast to the rubble and sea- grass substrates elsewhere but were devoid of coralliths. Encrusting colonies on the unstable substrates have a mean surface area of only 12.9 cm 2 (Fig. 11) at develop- ment stage 3 with a maximum of 22 cm 2. Stages 4 and 5, which attain mean sizes of 23.2 cm 2 and 30.5 cm 2 respec- tively, are both free living coralliths. Thus the only large size colonies on the rubble bo t tom are free living coral- liths. I t is concluded a spherical shape enables colonies of S. radians to grow larger in a disturbed habitat and hence has a selective survival advantage.

Acknowledgements. I am grateful to Paul Snelgrove for technical assis- tance and to Dr. Wayne Hunte for laboratory facilities at the Bellairs Re- search Institute of McGili University in Barbados. The research was sup- ported by a grant from the Natural Sciences and Engineering Research Council of Canada.

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