Lime-boring algae in hermatypic coral skeletons

267

J. exp. mar. Biol. Ecol., 1981, Vol. 55, pp. 267-281 Elsevier/North-Holland Biomedical Press

LIME-BORING

ALGAE

IN HERMATYPIC

RAYMOND

CORAL

SKELETONS

C. HIGHSMITH

Dc,p~rtment qf Zoology, Universit.v of Washington, Seattle, Washington, U.S.A. Abstract: Measurements on the green bands produced by endolithic algae in the genus Ostreohium (Chlorophyta: Siphonales) within massive coral skeletons indicate: (1) that the algal bands are farther from the skeletal surface in the tops than sides of heads; (2) that multiple algal bands in Porita lutea Milne Edwards & Haime have a periodicity (9.5 mm) slightly greater than but within the range of mean annual P. lutea growth rate (x =7.6 mm/yr, range: 3.5511.8 mm/yr); (3) that algal bands are farther from the skeletal surface in corals with high bulk density, probably because such skeletons transmit more light than low-density skeletons; (4) that the distance of the algal band from the skeletal surface is inversely correlated with water depth in some corals; and (5) that the distance between the algal band and skeletal surface is not correlated with individual coral growth rates. Calcite. reported to occur in P. lobata Dana and known to precipitate on algal filaments in marine sediments, was not detected in the skeletons of P. lutea, Favia pallida (Dana) or Goniastrea retiformi.~ (Lamarck), suggesting that Ostreobium is not a template for calcite formation in live corals.

INTRODUCTION

Some remarkably contradictory statements have been made about “lime-boring” algae, particularly Ostreobium spp. (Chlorophyta : Siphonales) in coral skeletons. Duerden (1902), based on many observations, reported the universal occurrence of boring algae in corals and suggested that algal corrosion was perhaps the most important agent of coral skeletal disintegration. Likewise, Gardiner (1930, 1931) was of the opinion that boring algae were the “primary and chief destructive agents of corals and coral rocks,

probably possessing an importance greater than that of On the other hand, Bertram (1936) all other boring organisms taken together”. ascribed no role to boring algae in the break-off of corals at Ghardaqa, Red Sea, estimating that breakage was due to boring sponges (x60%), boring molluscs ( z 20x),

defects

in growth

form

(= 10%)

and

grown

on an inadequate

base

( z 10%). Similarly, Golubic et al. (1975) reported that endolithic algae are restricted to the thin, photic zone within the substratum and are thus primarily a surface phenomenon. They concluded that “with no external interference, the cumulative effect of carbonate rock destruction by a stabilized subtidal endolithic (algal) community is minimal”. Odum & Odum (1955) reported that boring algae occur in all coral heads and, in complete contrast to Duerden (1902) and Gardiner (1930, 1931), suggested that these algae are beneficial, contributing to the survival and rapid growth of major reef-building corals as well as contributing significantly to 0022-098 l/S 1/OOOO-0000/$02.50

0 198 1 ElsevierjNorth-Holland

Biomedical

Press

268

RAYMONDC.HIGHSMITH

the high photosynthetic

activity

that there are often several innermost

shown

“healthy”

by most coral

green bands

band were at the compensation

point,

colonies.

present

They also stated

and surmised

the excess productivity

that if the of the upper

bands could be used by the coral. With regard to the occurrence

and productivity of the algae, Halldal (1968) reported that Ostreobium only occurred in x5;/, of Favia specimens examined in the Flinders Island Group, Great Barrier Reefs. Halldal (1968) and Shibata & Haxo (1969) also found that very little light penetrated to the uppermost green algal band in F. pallida and that there is probably not even enough light reaching the inner edge of the first green band to support photosynthesis and hence, the deeper bands were probably moribund. Kanwisher & Wainwright (1967) determined from measurements of respiration and light penetration that boring algae were not major producers in coral heads. They were only able to identify intact chloroplasts in the outermost band and found that the green pigment in deeper bands was largely phaeophytin, a degradation product of chlorophyll, liberated into the mineral of the skeleton. They concluded, therefore, that only the outermost band was living and that the deeper bands were photosynthetically inactive. Schroeder (1972) even suggested that Ostreobium lived heterotrophically and that the presence in the skeleton of compounds suitable for degradation by the algae would determine whether or not the coral was infested. Finally, Ostreobium may affect the mineral content of coral skeletons. Coral skeletons are generally composed of the aragonitic form of calcium carbonate (Chave, 1954; Kitano & Hood, 1965). Houck et al. (1975) found, however, high percentages of low-magnesium calcite in the skeletons of several Porites lobata in Hawaii. They hypothesized that the calcite was secreted by the corals but further study of the material (Macintyre & Towe, 1975) indicated that at least some of the calcite was associated with micro-borings. Based on measurements of algal damage to coral skeletons, the occurrence of calcite in skeletons, the size and position of algal bands relative to light penetration of different coral skeletons and to water depth, I propose alternative hypotheses on the distribution of Ostreobium within coral skeletons and also attempt to resolve some of the contradictions

mentioned

above.

MATERIALAND

METHODS

The massive corals Porites lutea, Favia pallida, Goniastrea retiftirmis, Platygyra lamellina, Pavona claws (Dana), Oulophyllia crispa, and Astreopora myriophthalma, were collected over a depth range of 0 to 30 m in the lagoon ,of Enewetak Atoll, Marshall Islands. A central slab parallel to the major growth axis was cut from each head (Highsmith, 1981a). The width of the green algal bands and their depth within the coral skeletons were measured on the slabs (Fig. 1).

LIME-BORING

A Varian

SuperScan

of light transmitted blocks,

Fig.

3 spectrophotometer

through

rectangular

2 x 1.2 cm in section,

1 Section of Goniastrra

ALGAE

was used to measure blocks

were cut from

rer(formis showing

269

IN CORALS

relative

amounts

cut from the coral skeletons. the surface

band of endolithic skeleton.

of the coral

algae (arrow)

The

to a depth

contained

within

the

of 4 cm and placed for 24 h in 5.25% HClO, diluted 507; with tap water to remove coral tissue. The blocks were stored in sea water. For measurement of light transmittance, they were submerged in sea water in individual glass containers. The end of each block that had been at the surface of the skeleton was always placed toward the light source. Light transmittance through the skeletal blocks was measured over a range of wavelengths from 350-750 nm. As most green bands are <4 cm from the surface of the skeleton,

the blocks were then cut down to a length

of 2 cm

and the measurements repeated. X-ray diffraction was used to determine whether coral skeletons contained calcite. Approximately 3 cm below the skeletal surface a sample of skeletal CaCO, was removed from several heads, powdered with a mortar and pestle, and mounted on glass slides. The slides were scanned over a 2 a angle range of 25532” on a Picker X-ray Spectrodiffractometer. This range includes the major aragonite (3.27 and 3.40 A) and calcite (3.03 A) peaks needed to estimate in the skeletons (Chave, 1954; Houck et al., 1975).

(+ 5’;/,) the percentage

of each

270

RAYMONDC. HIGHSMlTH RESULTSAND DISCUSSION

DAMAGETO CORALSKELETONS The effect of Ostreobium (Jeffrey, 1968; Lukas, 1974) a microscopic filamentous green alga, on the integrity of coral skeletons appears to be minimal. In spite Qf its occurrence in every coral, I detected no cumulative, macro-scale damage attributable to Ostreobium spp. in any coral head in this study. (Measurements of bioerosion in these corals by various organisms are reported in Highsmith, 1981a.) There is only one quantitative report of damage (removal of CaCO,) to coral skeletons by Ostreobium. Kanwisher & Wainwright (1967) calculated that in the darkest green zones in Dichocoeniu stokesii, the skeletal mineral contained 12% by volume of algae. Since the density of solid aragonite is 2.94 and the bulk density of D. stokesii is ~2.0 (Highsmith, 1979a), the reduction in bulk density of the coral in the algal bands would be ~8%. Although algal filaments occur outside bands (Duerden, 1902; Odum & Odum, 1955; Urish, 1976), the percentage volume is surely less. The algal bands are also usually less than half the thickness of green band-white band couplets (see Table II) so an overall reduction in bulk density of ~4% is a reasonably conservative estimate. This would increase the skeletal porosity from 32 to 35x, theoretically reducing the skeletal fracture strength by x 2.5 MN/m’, or x 6% (Chamberlain, 1978). Furthermore, CaCO, may eventually precipitate in the micro-borings (Macintyre & Towe, 1975; Chamberlain, 1978) so that net reduction in skeletal strength is probably quite small. ALGAL BANDMEASUREMENTSWITHIN SPECIES All corals examined contained at least one green band (Fig. 1) within the skeleton. In Goniastrea retifbrmis, Favia pallida, and Porites lutea, the mean distance from the outer edge of the uppermost algal band to the skeletal surface (Table I) was greater in the tops than the sides of the heads. (In all three species P < 0.005 ; Wilcoxon matched-pairs signed-ranks tests.) The other species were not analysed statistically because sample sizes were too small, but they showed a similar trend. The algal bands are also thicker in tops than in sides of heads in P. lutea (P -C0.01) and Favia pallida (P < 0.05) but not Goniastrea retiformis (Table I; Wilcoxon matched-pairs signed-ranks tests). This difference in the depth of the algal band within a skeleton is probably due to greater light penetration in the tops of heads.

LIME-BORING

ALGAE

IN CORALS

271

TABLE I

Mean distance (X) from outer edge of first Ostreobium band to skeletal surface and mean band for tops and sides of coral heads: n = no. of heads, 34 measurements per head average. Sides

Top X (mm)

Range

(mm)

?I

Goniustrea retiformis (Lamarck) Distance 16.0 4.629.7 Width 4.2 2.3- 6.0 Porites lutra Milne Edwards & Haime Distance 3.9 0.7-l 1.7 Width 2.4 1.6 4.5 Fuviu pallida (Dana) Distance 4.2 g13.5 Width 5.1 3.3- 7.5 PlatJagyra lamellina Ehrenberg Distance 7.9 4.5-14.0 Width 5.7 3.3- 8.0 Astreopora myriophthalma (Lamarck) Distance 5.0 2.3- 7.6 Width 4.1 3.8- 4.3 OdophJdiu crispa (Lamarck) Distance 6.0 Width 4.0 _

MULTIPLE

ALGAL

width

X (mm)

Range (mm)

4.9 4.2

1.6-12.0 2.0- 8.5

2.6 2.0

1.5- 5.7 l.o- 3.0

0.3 3.4

t& 1.0 l.O- 7.0

3.0 3.6

l.O- 5.0 3.0- 4.0

F, 9

12

8

4

No live coral tissue on sides

I 2.5

_

4.5

BANDS

Two Goniastrea retiformis, three Favia pallida, and five Porites lutea heads had from two to four additional bands deeper in the skeleton. All bands were green but deeper bands tended to have gaps or to be incomplete. In P. lutea with more than one band (Table II), the mean distance between bands was 7.3 mm. Thus, the Wean thickness of a white band-green band couplet was 9.5 mm (7.3 + 2.2 mm).

TABLE II Multiple

Distance Distance Distance Distance Distance

algal bands: mean band width and mean distance between bands measured from edge of a band to the outer edge of the next deeper band in Porites lutea.

between between between between between

all bands 1st and 2nd 2nd and 3rd 3rd and 4th 4th and 5th

Band width, all bands

bands bands bands bands

the lower

X (mm)

Range (mm)

No. of heads

7.3 10.5 5.9 7.2 3.5

3.0-14.3 6.6-14.3 4.5-10.0 3.0-14.0 3.0- 4.0

5 5 5 3 2

2.2

l.O- 3.5

5

212

The mean

RAYMOND

linear

of 3.5-l 1.8 mm/yr periodicity

growth

rate of P. lutea at Enewetak

(Highsmith,

of x l-l.4

C. HIGHSMITH

1979b). This suggests

yr. I do not know why multiple

is 7.6 mm/yr that

band

bands

with a range

formation

has a

were not evident

in

all heads; many had green spots or faded yellow locations in the skeleton that may have been remnants of other bands. In Porites astreoides at Curacao, Roos (1967) reported the “zone of boring algae In Enewetak corals, Buddemeier et al. was present only from May to September”. (1974) interpreted multiple algal bands as an indication that boring algae periodically re-infest corals. They showed (their Fig. 6) a Goniastrea ret$wmis with a growth rate of 6 mm/yr that has two algal bands 2-2.5 cm apart. These are obviously not annual bands. In the Contreras Islands, on the Pacific side of Panama, multiple

Fig. 2. Gardincrosrris

plunulara

section

showing over 40 green bands: Panama, by P. W. Glynn.

specimen

collected

at Isla Uva,

LIME-BORING

green bands intervals

in large specimens

as judged

by annual

ALGAE IN CORALS

213

of Gardineroserisplanulata (Dana) density

variations

in the coral skeleton

occur

at x I-yr

(Fig. 2; P. W.

Glynn pers. comm.). On the other hand, Lukas (1973) suggested that Ostreohium penetrates coral skeletons shortly after metamorphosis and grows (bores) as the coral grows. 1 have collected Goniastrea retifbrmis stained a light yellow-green from the single green band down to the base of the skeleton. Above the green band, the skeleton was white. This suggests, in agreement with Lukas (1973), that the endolithic algae simply grow upward, with photosynthetic pigment concentrated along the growing edge, Duerden (1902), Odum & Odum (1955) and Urish (1976) also found algal filaments in skeletal locations other than green bands. Thus, multiple green bands are an enigma. If the algae grow apace with the coral, why is there more than one band? Or, if bands are produced during a particular season why do not all corals have green bands approximately one year’s growth apart? On the other hand, if multiple bands are due to re-infestation, some heads may not be colonized each year but this possibility does not explain the presence of filaments between bands or why nearly every coral skeleton studied contained a green band near the surface. Perhaps differential decomposition of algal pigments in deeper bands is responsible for the difficulty in interpreting multiple banding. This explanation suffers because some green bands, although moribund, remain visible for many years, as judged by their distance from the skeletal surface (Fig. 2), so it is hard to understand why the majority of corals in this study have only a single recognizable band. ALGAL

BAND MEASUREMENTS:

The algal bands

BETWEEN

in tops of heads

SPECIES DIFFERENCES

(Table

I) are thicker

in Favia pallida than

in

Porites lutea (P ~0.001) but not Goniastrea retlfbrmis (P = 0.075) and thicker in G. retlfbrmis than in Porites lutea (P < 0.001; Mann-Whitney U-tests). The algal bands are, also, farther from the upper skeletal surface in Goniastrea ret~fbrmis than in either Porites lutea (P < 0.001) or Favia pallida (P < 0.001 ; Mann-Whitney U-tests). The latter difference is surprising since the Goniastrea retlfbrmis skeleton is z 2Oq, denser than Porites lutea or Favia pallida (1.7 vs. 1.4; Highsmith, 198 la). Furthermore, the algal band in a specimen of Pavona claws (bulk density x 1.9; Highsmith, 1979a) averaged 23 mm from the upper surface. LIGHT PENETRATION

OF CORAL SKELETON

To test the hypothesis that light penetrates farther into coral skeletons of high bulk density than into more porous skeletons, I measured relative light transmittance through pieces of skeleton from different species in a series of side-by-side comparisons. Generally, more light was transmitted through Goniastrea ret{fhmis than through Porites lutea, Favia pallida or Oulopl~~~llia crispa skeletons (Table III). In addition, more light was transmitted through Pavona claws than through

TABLE

III

40 20 40 40 20 40 20 40 20

Coral species B

Goniastrea retiformis (1.7) Goniastrea rettformis (1.7) Porites lutea (1.4) Porites lutea (1.4) Porites lutea (1.4) Favia pallida (1.4) Favia pallida (1.4) Oulophyllia crispa (0.85) Oulophyllia crispa (0.85)

Coral species A

Pavona claws (1.9) Pavona claws (1.9) Pavona claws (1.9) Goniastrea retiformis (1.7) Goniastrea ret!formis (1.7) Goniastrea ret[formis (1.7) Goniastrea retiformis (1.7) Goniastrea retiformis (1.7) Goniastrea retiformis (1.7)

19 24 4 30 16* 19 13* 4 8

n

8

1

16 24 4 19 10 11 11

A >B

A
0 0 8 2 1 0 3 0

0

A=B


< 0.005 . <0.025 < 0.02 <0.01 13.4 6.5 8.1 6.2

(A >B)

Significance

8.9 24.0

Chi-square

light transmittance through pairs of cleaned, rectangular blocks of coral skeleton of different bulk density: density given in parentheses for *, includes four difference spectra where more light was transmitted through A in the long wavelength end of the spectrum and through B for short wavelengths; two were included in the A > B category and two in the A
Comparative each species;

LIME-BORING

ALGAE

IN CORALS

275

Goniastrea retiformis or Porites Iutea (Table III). In a few cases, mixed results were obtained; Goniastrea retiformis transmitted more light in the upper 100-200 nm of the spectrum scanned (350-750 nm) than Porites lutea or Faviapallida and vice versa for shorter wavelengths. Perhaps dense skeletons transmit long wavelengths more effectively than short wavelengths. The skeletal bulk density of corals is a function of corallite wall thickness relative to corallite diameter (Highsmith, 1981b). Therefore, I hypothesized that corallite walls act as light tubes (Fig. 3), i.e. total internal reflection occurs and light is Light

Fig. 3. Diagrammatic section of cerioid (neighboring corallites have a common wall) coral skeleton parallel to direction of growth: light is reflected fewer times as it descends a corallite with thick walls (A) than in a corallite with thin walls (B) so light of equivalent intensity penetrates deeper in skeleton A ; the light pathways shown are of equal length.

transmitted down corallite walls into the skeleton. Absorption spectra for F. pallida (Shibata & Haxo, 1969) imply that white light is transmitted through skeletal ridges, i.e. corallite wall termini (Fig. 3), on the surface of the skeleton. The polyps of the species reported on here tend to be contracted during the day. Consequently, less light is probably absorbed by zooxanthellae in coral tissue drawn over the intercalicular ridges than by zooxanthellae in tissues contracted down into the calices. Because long wavelengths have a slightly higher reflectivity than short wavelengths and are also less likely to be scattered by objects in their path (Tolansky, 1965), spectral differences in reflectivity and scattering may account for the mixed results mentioned above.

216

RAYMOND

C. HIGHSMITH

In corals of low bulk density (high porosity), the thin corallite walls are evidently not effective light transmitters. Theoretically, light should not penetrate as far into low density skeletons because more reflections per unit length of corallite would occur in thin walls than in thick walls (Fig. 3). Thus, light would have to travel farther in thin-walled than thick-walled corallites to penetrate the same distance into the skeleton and light absorption increases logarithmically with path length (Tolansky, 1965). Differences in skeletal architecture may also be involved. Both Goniustrea rehformis and Favia pallida have long, straight corallites that extend well into the skeleton but Porites lutea does not (see Fig. 4 in Highsmith, 1981a). Furthermore, a smaller proportion of incident light will strike the thin intercalicular ridges of low-density skeletons, i.e. low-density skeletons have relatively less light receiving surface area. Shibata & Haxo (in Halldal, 1968) found the percentage of light reaching the top of the outermost algal band in live Favia pallida was O.lO-0.15x, 0.6%, and 2.0% for wavelengths of 340-680 nm, 700 nm, and 720 nm, respectively. Action spectra of photosynthesis for zooxanthellae isolated from F. pallida tissues revealed that they were utilizing light in the 30&680 nm range, which is probably why so little light of these wavelengths reached the algal band. Ostreobium from Favia pallida gave a similar action spectrum except that it also

Fig. 4. Back-lighted

section

of Goniastrea retiformis showing step change algal band in the center of the head.

in the depth of the endolithic

LIME-BORING

responded percentage thellae

strongly

to light between

of light in the longer

layer,

(2) is transmitted

ALGAE

680 and 720 nm (Halldal,

wavelengths through

277

IN CORALS

(1) passes

the skeleton

1968). Thus, a higher

through (especially

the coral-zooxanif thick corallite

walls are present), and (3) is utilized by algae in the green band. The endolithic algae are so adapted to conditions inside coral

skeletons

that

they reach photosynthetic saturation at light levels as low as 1000 erg .crn-’ .s’ or less (Halldal, 1968). Although the outer edge of the algal band did not show photosynthetic inhibition at intensities as high as 5000 erg. cm-’ . SK’, the center of the band was photo-oxidized by blue light at intensities > 1800 erg 1cm-’ . SC’ (Halldal, 1968) which is x0.004 of incident light at the earth’s surface on a sunny day in the tropics (Shibata & Haxo, 1969). This probably explains why algal bands are farther from the surface in corals with skeletons that transmit more light; not only is there suflicient light deeper but there may be too much light nearer the surface. This explanation is supported by the configuration of the algal band in Fig. 4. In the center of the head where corallites are vertical and presumably transmit the most light, the algal band shows a step-change in distance from the skeletal surface. On the sides of heads, the angle of incidence may be too great for light to be reflected within the corallite walls. LOCATION

OF ALGAL

BANDS RELATIVE

TO WATER DEPTH

Because light intensity declines exponentially with water depth (Houck, et al., 1977), the algal bands should be closer to the skeletal surface in corals from increasingly deeper water. For Porites lutea, Goniastrea retiformis and Favia pallida combined, the distance from the upper surface of the coral skeleton to the top of the outermost algal band is inversely correlated with water depth (P < 0.05, r, = 0.32, n = 37; Spearman rank correlation coefficient). There is, however, considerable variability in the positions of the algal bands (Fig. 5). Because of this variability and small sample sizes, Porites Iutea (r, = 0.11, n = 17) and Goniastrea rehformis (r, = 0.33, n = 10) do not give significant correlations when considered separately, although Favia pallida does (P < 0.05, r, = 0.63, n = 10). These data, combined with the positive correlation between skeletal bulk density and distance of the algal band from the surface of the skeleton, indicate that Ostreobium is at least partly, if not entirely, autotrophic. The position of the algal band in Porites lutea is not inversely correlated’with water depth because the bands were close to the skeletal surface in heads collected from shallow water. Thus, light attenuation due to skeletal opacity in P. lutea (see p. 273) appears to be more significant than that due to increased water depth. More generally, the location of algal bands in corals with low bulk densities and lacking relatively long, straight corallites, may not be related to water depth because the algal bands will only receive sufficient light near the surface of the skeleton. The abundance of filaments in algal bands, however, may be reduced in deeper

278

RAYMOND

C. HIGHSMITH

water (Urish, 1976). For Porites lutea, I tested the possibility that some of the variability in algal band position was due to differences in growth rates of the corals, which are also highly variable (Highsmith, 1979b). They were not significantly correlated (r, = 0.18, n = 12).

IO 15 Wafer Depth (ml

Fig. 5. Distance

between

coral

skeletal

surface function

and the outer margin of water depth.

of the nearest

algal

band

as a

Another possible source of variability is that within coral species, skeletal bulk density tends to increase with water depth (Drew, 1973; Baker, 1975; Highsmith, 1979b). Thus, coral skeletons from deep water may transmit light more effectively than those from shallow water. Response to light, as mediated by coral skeletal density and/or architecture and water depth, appears to be a major factor in determining the size and position of Ostrebium bands. SKELETAL

CALCITE

CONTENT

In coral reef substrata, high-magnesium calcite commonly precipitates around filaments of boring algae (Alexandersson, 1972; Schroeder, 1972). Furthermore, periostracum transplant experiments in a gastropod mollusc revealed that the template upon which CaCO, precipitates affects the crystal type formed (Meenakshi et al., 1974). These reports suggest the hypothesis that low-magnesium calcite (aragonite has low-magnesium content) may precipitate around Ostreobium filaments in Porites lutea where the algal band is often adjacent to the growing surface of the skeleton. Algal filaments extending onto the surface or into pore spaces, which are interconnected and not necessarily isolated from the surface in P. Zutea, might well serve as nucleation sites for low-magnesium calcite in an environment strongly favoring CaCO, precipitation. Conversely, calcite should not be present in Goniastrea retiformis, at least in the center of colonies, because the Ostreobium band is usually well separated from the zone of skeletogenesis (Table I).

219

LIME-BORINGALGAEINCORALS

X-ray Goniastrea

diffraction retiformis,

analysis

of skeletal

samples

from

and three Favia pallida indicated

calcite were not present

in any of the specimens

six Porites

that significant

tested,

i.e. the major

lutea,

three

amounts

of

calcite peak

(3.03 A) was not produced. As the mean calcite content in Porites lobata was 24% (Houck et al., 1975) and I was testing for a general phenomenon, the X-ray diffraction study was terminated. The hypothesis is incorrect either because CaCO, precipitation around the algal filaments simply does not occur in this situation, at least not as calcite, or because the algal filaments were confined within skeletal mineral and did not extend into pores. In regard to the latter possibility, Duerden (1902) Odum & Odum (1955) Schroeder (1972) and Lukas (1974) reported algal filaments at least occasionally entered pores whereas Kanwisher & Wainwright (1967) and Alexandersson from the mineral.

(1972) found

endolithic

algae tended

to avoid

emerging

CONCLUSIONS

Ostreobium is probably not a substratum for the precipitation of calcite in coral skeletons at Enewetak, at least not during the coral’s most recent 4-5 yr of primary skeletal deposition. The development of highly pigmented algal. bands presumably occurs where and when conditions within a coral skeleton are optimal for vigorous growth, perhaps analogous to phytoplankton blooms where small populations expand rapidly when the proper conditions of light, temperature and nutrient concentrations co-occur. Three major factors appear to affect the intensity and spectral quality of light available to Ostreobium living within coral skeletons. First, the zooxanthellae in coral tissue absorb or screen out 98% or more of the incident light, especially in the photosynthetically important wavelengths between 340-680 nm; as little as 0.1% of incident light in these wavelengths may penetrate (Kanwisher & Wainwright, 1967; Halldal, 1968). Secondly, the bulk density and internal architecture of coral skeletons affects the distance light is transmitted into them. Dense skeletons with thick corallite walls transmit light deeper than less dense skeletons, although extremely

porous

skeletons

may also permit increased

light penetration,

as suggested

by the results for 40 mm Oulophyllia crispa (Table III). Thirdly, light intensity declines exponentially with increasing water depth and absorbancy of long wavelengths as water depth increases is greater than for short wavelengths (Dustan, 1979) in contrast to factors 1 and 2. The above factors combined with the findings of Halldal (1968) that Ostreobium (1) saturates at very low light intensities, (2) is photo-oxidized at quite low light intensities and (3) utilizes light of longer wavelength than the overlying zooxanthellae, appear to determine the position of algal bands in coral skeletons. This interpretation does not, however, account for multiple algal bands in some coral skeletons.

280

RAYMOND C. HIGHSMITH

An alternative surface

interpretation

of the coral skeleton,

by recruitment,

is that green bands either

so that the position

by seasonal

are produced growth

annually

of the resident

of the outer band is a function

near the alga(e)

or

of when the band

was produced relative to the growth rate of the coral. Evidence in Kanwisher & Wainwright (1967), Roos (1967), Table II, and Fig. 2, tend to support this interpretation. Arguing against this hypothesis is the apparent lack of multiple bands in many heads. This could be explained by rapid fading of bands but some bands evidently persist for years (Table II, Fig. 2). Porites lutea (7.6 mm/yr) also grows faster than Goniastrea retiformis (6.8 mm/yr; Highsmith, 1979b) so the algal band should be farther from the surface in the former rather than closer (Table I). Furthermore, this interpretation does not explain the relationship between band position and skeletal density, configuration of the green band in Fig. 4, or the presence of algal filaments between bands (Duerden, 1902; Odum & Odum, 1955 ; Urish, 1976) in the case of annual recruitment. The data presented here and in the literature are not sufficient to choose between the above interpretations. It may never be possible to distinguish between recruitment and seasonal growth by resident algae, unless the life history of Ostreobium can be worked out, because filaments occur between the multiple green bands (see above) and because the multiple bands join or overlap along the sides of coral skeletons and thus, are never completely separated. It should, however, be possible experimentally to determine the relationship between light and algal band location in coral skeletons. ACKNOWLEDGEMENTS

I thank Dr. S. V. Smith for use of facilities at the Mid-Pacific Marine Laboratory. I am grateful to A. Riggs for field assistance, B. Aubrey, R. Ralf, and S. Schonberg for help with X-ray diffraction, manuscript, NSF grant Highsmith.

to Drs. A. J. Kohn

and R. T. Paine

for reading

the

and to an anonymous reviewer for helpful suggestions. Supported by no. OCE 76-21271, the Mid-Pacific Marine Laboratory, and D. D.

REFERENCES T., 1972. Micritization of carbonate particles: processes of precipitation and dissolution in modern shallow-marine sediments. Bull. Geol. Instn Univ. Uppsala, N. 5, Vol. 3, pp. 201-236. BAKER,P. A., 1975. Coral growth rate: variation with depth. M.S. thesis, Pennsylvania State University, State College, 11 pp. BERTRAM,G. C. L., 1936. Some aspects of the breakdown of coral at Ghardaqa, Red Sea. Proc. zool. Sot. Lond., Vol. 106, pp. 101l-1026. BUDDEMEIER,R. W., J.E. MARAGOS& D. W. KNUTSON, 1974. Radiographic studies of reef coral exoskeletons: rates and patterns of coral growth. J. exp. mar. Biol. Ecol., Vol. 14, pp. 179-200. CHAMBERLAIN, JR., J. A., 1978. Mechanical properties of coral skeleton: compressive strength and its adaptive significance. Paleobiology, Vol. 14, pp. 419-435.

ALEXANDERSSON,

LIME-BORING

ALGAE

IN CORALS

281

CHAVE, K. E., 1954. Aspects of the biogeochemistry of magnesium. I. Calcareous marine organisms. J. Geol., Vol. 62, pp. 266-283. DREW, E. A., 1973. The biology and physiology of alga-invertebrate symbioses. III. In situ measurements of photosynthesis and calcification in some hermatypic corals. J. exp. mar. Biol. Ecol., Vol. 13, pp. 165-179. DUE.RDEN, J. E., 1902. Boring algae as agents in the disintegration of corals. Bull. Am. Mus. Nat. H&r.. Vol. 16, pp. 323-332. DIJSTAU, P., 1979. Distribution of zooxanthellae and photosynthetic chloroplast pigments of the reefbuilding coral Montascrea annularis Ellis and Solander in relation to depth on a West Indian coral reef. Bull. mar. Sci., Vol. 29, pp. 79-95. GARDINER, J. S., 1930. Photosynthesis and solution in formation of coral reefs. Proc. Linn. Sot. Lond.. 193031, Pt. 5, pp. 65-71. GARDINER, J. S., 1931. Coral reefs and a/oils. Macmillan, London, 181 pp. Gotualc, S., R. PERKINS & K. LUKAS, 1975. Boring microorganisms and microborings in carbonate substrates. In, The study of trace fossils, edited by R. W. Frey, Springer-Verlag, New York. pp. 229-259. HAL.LDAL, P., 1968. Photosynthetic capacities and photosynthetic action spectra of endozoic algae of the massive coral Favia. Biol. Bull. mar. biol. Lab.. Woods Hole. Vol. 134, pp. 41 l-424. HIGHSMITH, R.C., 1979a. Corals: the inside story. Ph.D. thesis, University of Washington, Seattle. 321 pp. HI(;HSMITH, R.C., 1979b. Coral growth rates and environmental control of density banding. J. exp. mar. Biol. Ecol., Vol. 37, pp. 105-125. HIGHSMITH, R. C., 1981a. Coral bioerosion at Enewetak: agents and dynamics. Int. Revue ges. Hxdrohrol.. Vol. 66. pp. 335-375. HIGHSMITH, R. C., 1981b. Coral bioerosion: damage relative to skeletal density. Am. Nat., Vol. 117. pp. 193-198. HOIJCK, J. E., R. W. BUDDEMEIER & K.E. CHAVE, 1975. Skeletal low-magnesium calcite in living scleractinian corals. Science, Vol. 189, pp. 997-999. HOUCK, J. E., R. W. BUDDEMEIER, S. V. SMITH & P. L. JOKIEL, 1977. The response of coral growth rate and skeletal strontium content to light intensity and water temperature. Proc. 3rd inr. Coral Reef Symp., Vol. 2, Rosenstiel School of Marine and Atmospheric Science, Miami. U.S.A.. pp. 425-431. JFFf;REY, S. W., 1968. Pigment composition of siphonales algae in the brain coral Favia. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 135, pp. 141-148. KANWISHER. J. W. & S. A. WAINWRIC;HT, 1967. Oxygen balance in some reef corals. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 133, pp. 378-390. KIT~NO. Y. & D. W. HOOD, 1965. The influence of organic material on the polymorphic crystallization of calcium carbonate. Geochim. Cosmochim. Acta, Vol. 29, pp. 2941. LUKAS, K. J., 1973. Taxonomy and ecology of the endolithic microflora of reef corals with a review of the literature on endolithic microphytes. Ph.D. thesis, University of Rhode Island, Kingston. 159 pp. LUKAS, K. J., 1974. Two species of the chlorophyte genus Ostreobium from skeletons of Atlantic and Caribbean reef corals. J. Phycol., Vol. 10, pp. 331-335. M.4CINTYRE. I. G. & K. M. TOWE, 1975. Skeletal calcite in living scleractinian corals: microboring fillings, not primary skeletal deposits. ScirTnce, Vol. 193, pp. 701-702. MEENAKSHI, V. R., G. DONNARY, P. L. BLACKWELDER & K. M. WILRUR, 1974. The influence of substrata on calcification patterns in molluscan shell. Calc. Tiss. Res., Vol. 15, pp. 31-44. ODIJM. H.T. & E. P. ODLM. 1955. Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol. Monogr., Vol. 25, pp. 291-320. Roos, P. J., 1967. Growth and occurrence of the reef coral Porites astreoides Lamarck in relation to submarine radiance distribution. Drukkerij Elinkwijk, Utrecht, 72 pp. SCHROEDER, J. H., 1972. Calcified filaments of an endolithic alga in recent Bermuda reefs. N. Jb. Geol. Palaont. Mh, Vol. 1, pp. 16-33. SHIHATA, K. & F. T. HAXO, 1969. Light transmission and spectral distribution through epi- and endozoic alga1 layers in the brain coral, Favia. Biol. Bull. mar. biol. Lab., Woods Hole, Vol. 136, pp. 461-468. TOLANSKY. S., 1965. Curiosities qflight rays and light waves. American Elsevier. New York, 109 pp. URISH, C. L., 1976. Microfloral borers in recent Caribbean scleractinian corals. M.A. thesis, Rice University. Houston, 103 pp.