Coral Reefs (1996) 15:101-107 Coral © Springer-Verlag t996 e~

Experimental studies of rapid bioerosion of coral reefs in the Galfipagos Islands M. L. Reaka-Kudla 1, J. S. Feingold 2, W. Glynn 3

1 Department of Zoology, The University of Maryland, College Park, Maryland 20742 g Department of Math, Science and Technology, Nova Southeastern University, 3301 College Avenue, Ft. Lauderdaie, Florida 33029 3 Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, 4600 Rickenbacker Causeway, Miami, Florida 33149

Accepted: 29 December 1995

Abstract. Experimental carbonate blocks of coral skeleton, Porites lobata (PL), and cathedral limestone (LS) were deployed for 14.8 months at shallow (5-6m) and deep ( l l -13m) depths on a severely bioeroded coral reef, Champion Island, Galfipagos Islands, Ecuador. Sea ur- chins (Eucidaris thouarsii) were significantly more abun- dant at shallow versus deep sites. Porites lobata blocks lost an average of 25.4 kg m- 2 yr- 1 (23.71 m - 2 yr- 1 or 60.5 % decrease yr 1). Losses did not vary significantly at depths tested. Internal bioeroders excavated an average of 2 .6kgm-2yr 1 (2.41m-2yr 1 or 0.6% decrease yr-1), while external bioeroders removed an average of 22 .8kgm-2yr ~ (21.31m-2yr -1 or 59.9% decrease yr- 1); few encrusting organisms were observed on the PL blocks. Cathedral limestone blocks lost an average of 4 .1kgm-Zyr -1 (1.81m-2yr -1 or 4.6% decrease yr-t) , also with no relation to depth. Internal bioeroders ex- cavated an average of 0.6 kg m 2 yr- 1 (0.3 1 m - 2 yr - 1 or 0.7% decrease yr-1), and external bioeroders removed an average of 3 .5kgm-2yr -1 (1.51m 2yr-1 or 3.9% de- crease yr-1) from the LS blocks. Most (57.6%) encrusta- tion occurred on the bottom of LS blocks, and there was more accretion on block bottoms in deep (61.4 mg cm - 2 yr- 1) 'versus shallow (35.0 mg cm - 2 yr- 1) sites. External bioerosion reduced the average height of the reef framework by 0.2 cm yr-1 for hard substrata (repre- sented by LS) and 2.3 cm yr 1 for soft substrata (represen- ted by PL). The results of this study suggest that coral reef frameworks in the Galfipagos Islands are in serious jeop- ardy. If rates of coral recruitment do not increase, and if rates of bioerosion do not decline, coral reefs in the Galfipagos Islands could be eliminated entirely.

Introduction

The persistence of coral reefs in illuminated tropical waters depends upon a balance between the deposition and re-

Correspondence to: M. L. Reaka-Kudla

moval of calcium carbonate. Carbonate is lost from reef frameworks primarily through the actions of boring and scraping organisms-bioerosion (Risk and MacGeachy 1978; Trudgill 1983; Macintyre 1984; Hutchings 1986). Bioeroders also weaken the structural integrity of the reef so that corals and large pieces of framework are toppled by disturbances (storms, currents, or even the impacts of anchors) and subsequently break down (Scott and Risk 1988; Colgan 1990). Bioeroded sand and rubble may be shifted off the reef by gravity (sand chutes) or currents, and scouring can further engrave the topography of the reef. Sediments also can smother sessile organisms and adverse- ly affect reef growth. Thus, if not offset by calcification and consolidation, bioerosion can initiate a cascade of events that considerably alter the three-dimensional structure of the reef.

Erosion that is sufficiently rapid to be detected by casual observation of reef topography over a brief period is not common, except following major catastrophes such as severe hurricanes (Woodley et al. 1981) or pollution (Rose and Risk 1985; Jokiel 1986). Nevertheless, we have ob- served dramatic changes in the configuration of an entire reef framework over several years on Champion Island (Fig. 1), a small island northeast of Floreana Island in the Galfipagos Islands, Ecuador (Fig. 2). These changes may have resulted from low carbonate deposition, high bioero- sion or both of these factors acting in combination.

The objective of the present study was to quantify rates of bioerosion on the reef at Champion Island, and to ascertain what amount was caused by external scraping organisms (fishes and sea urchins) versus internal bio- eroders (primarily bivalves, sponges, and polychaete and sipunculan worms). We also estimated carbonate deposi- tion by encrustation (primarily by serpulid polychaetes, bivalves, foraminiferans, bryozoans, and coralline algae) that might potentially offset bioerosion. Champion Island was chosen as the location for this study because rapid erosion of the reef had been observed there since the 1982-1983 E1 Nifio Southern Oscillation (ENSO) event (Macintyre et al. 1992; Glynn 1994). During the study, the three-dimensional topography of the reef changed so dras-

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Fig. 1. View of a severely bioeroded colony of Pavona clavus, Champion Island, Galfipagos Islands, Ecuador (5 m depth, 3 June 1992). Note numerous Eucidaris thouarsii on coral rubble and remaining framework. Prior to the 1982-1983 E1 Nifio, this colony was alive and was 3 m high and 4 m in diameter

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Fig. 2. Location of the study site at Champion Island (inset), north coast of Floreana Island, Galfipagos Islands, Ecuador. Dotted lines indicate depth contours in meters. The location of the Charles Darwin Research Station (CDRS) on Santa Cruz Island is also indicated

t ical ly b e t w e e n the b e g i n n i n g (Apri l 1989) and the end (July 1990) of the e x p e r i m e n t t ha t it was difficult to r ecog- nize the p r e v i o u s l y m a p p e d m i c r o g e o g r a p h y a n d re loca te the s tudy sites.

Methods

Two large colonies of Porites lobata Dana (PL) (> 1 m in diameter and containing very few holes from internal bioeroders) from the highest reaches of the sand beach of Cormorant Bay on the northeast side of Floreana Island provided the material for the experimental blocks that were deployed on the reef at Champion Island. The colonies contained fresh, non-eroded calyces, indicating that they had been toppled while alive and tossed high onto the beach by storm generated waves from the west (the opposite direction from normal) during the unusually high sea level stands associated with the 1982-1983 ENSO event (Robinson 1985).

Colonies were cut with a hand saw into blocks approximately 4 x 8 x 8 cm in size, and a hole 9.5 mm in diameter was drilled vertically through the center of each block. The exact dimensions of all six sides of each block were traced onto a sheet of paper, and an intricate map of the size and position of any pre-existing bioeroded holes or other fissures, as well as the central drilled hole, was drawn onto each of the six sides of the tracing. The scale and position of these characteristics were recorded with a small hand-held copying machine.

The external dimensions of each PL block were recorded and surface areas were quantified by computer digitization at the Univer- sity of Maryland. These surface areas were converted to volumes. Pre-existing internal bioerosion in the selected coral skeleton was minimal (0.64% _+ 0.21 standard error, SE). Holes, fissures and bro- ken edges were subtracted from the total volume obtained. To estimate the volume of pre-existing internal bioerosion, we assumed that voids were distributed randomly throughout the block and that the six sides- cutting across the block in three different p lanes- comprised representative samples of the amount of carbonate miss- ing from the block prior to deployment.

Density of the Porites lobata skeleton was determined at the University of Maryland by sawing 11 cubes (2 x 2cm) from two colonies of P. lobata that were used to make the experimental blocks (five cubes were from one colony and six from the other). The cubes were scrutinized and any cubes containing borings, cracks, or other imperfections were discarded. The exact dimensions of the cubes were measured with calipers (two vertical and two horizontal measurements were made to the nearest 0.1 mm on each of the six

103

sides of each cube), the volume of each cube was calculated, and the mass of each dried cube was determined to the nearest mg on an analytical balance after drying at 150°C until they had reached a constant mass. The mass and volume of the cubes established the density of P. lobata skeleton (1.07 g cm- 3 +_ 0.04 SE). Using the den- sity and the "net" volume of each block (the total volume less all holes, fissures, or broken edges, as described above), the mass of each experimental PL block prior to deployment was calculated.

In order to simulate the harder, denser reef pavement that sup- ports corals in many areas, blocks of cathedral limestone (LS) were retrieved from fragments of Jurassic limestone that had been dis- carded during construction of the Washington National Cathedral. These fragments were cut with a rock saw (ca. 4 x 8 x 8 cm) and holes (9.5 mm diameter) were drilled in their center. The hardness of LS was slightly greater than 5, in contrast to values be'~ween 2 and 3 for PL blocks (Mohs relative hardness scale, Klein and Hurlbut 1977). The LS blocks were weighed after drying to a constant mass using the methods described above. They contained no pre-existing fissures or bioeroded holes. The density of the LS blocks was 2.28 g c m - 3 + 0.01 SE, as calculated from the mass (558.31 g + 3.76 SE) and volume (244.001 _+ 1.53 SE) of all pre- experimental LS blocks.

Six 1 x 1 m frames were constructed from PVC pipe (19.1 mm in diameter). For each frame, the pipes were arranged in an outer square with two bisecting cross bars, providing sites for the attachment of nine blocks (at the corner or intersection of each perpendicular set of pipes). A stainless steel bolt (9.5 mm diameter) was inserted through holes in the pipe and the blocks and capped with a nylon washer and a stainless steel nut. All blocks (PL and LS) were randomized and numbered. The positions of three PL blocks and six LS blocks were located on each frame using random numbers. Each frame was permanently numbered and the position of each block was recorded.

Three frames (each containing nine blocks) were anchored to the reef framework (with iron rebar stakes, nylon tie-wraps, and heavy monofilament line) approximately 7m apart and parallel to the island shore about 25 m from a promontory on the western side of Champion Island at a depth of 5-6 m. The remaining three frames (with their blocks) were attached similarly to the reef at sites approxi- mately 7m apart about 25 m west of the first set of sites at 11-13 m depth. The latter sites, established at the edge of a steeply declining fore reef slope, were approximately parallel to the coastline of the island and the shallower three sites. An effort was made to anchor the frames with all blocks either touching or within 2-3 cm of the substratum so that both crawling and swimming bioeroders could reach them.

The frames were deployed on April 20, 1989, and retrieved on July 13, 1990, exposing the blocks for 14 months and three weeks. Most field bioerosion experiments require at least two years before 5-15 % of the experimental substratum is removed by bioerosion, yielding analyzable data that are comparable to other studies and conditions (Kiene 1988; Eakin 1992; Hutchings et al. 1992). However, bioero- sion of the PL blocks at Champion Island was so rapid that the experiment was terminated early.

Upon retrieval, 6 of the 18 PL blocks were missing from their frames and a segment of one frame supporting 3 LS blocks was lost. We concluded that the PL blocks were removed by bioerosion; the frames and bolts were intact, 10 of the remaining 12 blocks had lost 41 80% of their volume, and there were clear indications of scraping on remaining blocks. Since an entire frame segment of LS blocks was missing, and LS blocks experienced only 3 7% volume loss, we believe that they were mechanically removed, perhaps by sea lions or a boat anchor. Data from lost LS blocks therefore were excluded from all analyses.

All of the blocks were dried to a constant mass, photographed, and vertically slabbed (7-8 mm thickness) with the rock saw. The faces of the slabs were photocopied (using a state of the art, high resolution and high contrast machine) to record evidence of internal bioerosion. The area ofbioeroded holes was quantified relative to the total area of the slab with a computer digitizer to determine the percentage of carbonate removed by internal eroders (using the same assumptions described above). A m m ruler placed beside the slab on

the copier revealed less than 0.5% distortion in any sample, and no significant distortion was detected in 20 samples tested (paired t-test, p > 0.05). The slab always was placed in the center of the copy field. Each slab was examined visually adjacent to the copied image to verify all marks and identify any borings that were not revealed clearly on the photocopy. Since this method detected holes as small as the porosity of the coral, we believe that few or no borings were missed.

Bioerosion of the PL blocks was severe and little encrustation was observed. In contrast, the LS blocks retained most of their original size and considerable calcareous encrustation was observed on their surfaces. To determine the amount of carbonate accretion on the LS blocks, all encrustations were removed. Encrustations from each face of the blocks were placed into separate foil containers. The scraped block and the dislodged encrustations then were weighed individually to the nearest mg. Calcareous accretion was visually distinct from the underlying smooth gray limestone. These measure- ments yielded separate values for the amount of carbonate removed by bioerosion and the amount of carbonate added by encrustation.

For the PL blocks, few encrusting organisms were present and the measured post-experimental mass was subtracted from the pre- experimental mass (calculated from the measured volume and known density as described above). The post-experimental volume (calculated from the measured mass and the known density) was subtracted from the measured pre-experimental volume to obtain the volume of carbonate removed from each block.

The abundance of slate pencil sea urchins was assessed by throw- ing a 0.25 m 2 frame out of a boat to determine initial position and then placing the frame in random directions and distances to deter- mine subsequent positions.

Data were analyzed by parametric methods whenever possible. Homogeneity of variance was determined with the F test. When

max . appropriate, nested ANOVA and the t-test for samples wath unequal variance (t' test, Sokal and Rohlf 1969) was employed. The Kruskal- Wallis non-parametric test (Zar 1984) was employed for multiple comparisons when variances were heterogeneous.

Results

Bioeroders

D e n s e p o p u l a t i o n s of the slate penc i l sea u rch in Eucidaris thouarsii Valenc iennes were obse rved at C h a m p i o n Island. T h e y were g raz ing on b o t h l ive cora l and on f i l a m e n t o u s a n d o t h e r algae, and were s ign i f ican t ly m o r e a b u n d a n t in sha l low hab i t a t s t h a n on deepe r p o r t i o n s of the reef ( M a n n W h i t n e y U test, p < 0.001) (Fig. 3). A few Tripneustes ventricosa also were o b s e r v e d g raz ing on a lgae on d e a d reef surfaces. A l t h o u g h the la rge E. thouarsii were the m o s t a b u n d a n t g razers o b s e r v e d to feed on l ive a n d d e a d co ra l s u b s t r a t u m at the t ime of the s tudy (Fig. 3), cha rac t e r i s t i c g raz ing m a r k s of pa r ro t f i shes also were n o t e d on P L b locks at the t ime of the i r co l lec t ion , i nd i ca t i ng tha t fishes r e m o v e d c a r b o n a t e as well.

N u m e r o u s g raz ing fishes were o b s e r v e d at C h a m p i o n Is land, i n c l u d i n g fou r species of pa r ro t f i shes (Scarus per- rico, Scarus rubroviolaceus, Scarus 9hobban, Scarus com- pressus) and th ree species of tangs (Zanclus cornutus, Acanthurus nigricans, Prionurus laticlavius). Triggerf i shes , wh ich s o m e t i m e s bi te and b r e a k pieces of co ra l to o b t a i n i n v e r t e b r a t e s w i th in the ske le ton (Guzmf in a n d Cor t6s 1989), a lso were o b s e r v e d fo r ag ing n e a r the site. At least five species of t r iggerf ishes occu r in the Ga l f i pagos I s lands (Alutera scripta, Sufflamen verres, Pseudobalistes naufragium, Melichthys niger, and Xanthichthys mento), a l t h o u g h we

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22

Fig. 3. Abundance (mean _+ SE) of Eucidaris thouarsii at different depths at the study site, Champion Island, 17 June 1988. Numbers of urchins were significantly greater (Mann Whitney U test, U = 36.5, p< 0.001) and more variable (Fro, x = 3.56, p =0.02) in the 4 6m habitat (depth of the shallow blocks) than at 13 m (depth of the deep blocks)

have not observed the latter two species at Champion Island.

Of internal eroders, l i thophagid bivalves (including Lithophaga laevigata and Lithophaga aristata) were abun- dant in live coral at the study site (e.g., Porites Iobata). The surfaces of dead corals (e.g., those likely killed during the 1982-1983 ENSO) were densely pocked with the vacant holes of dead bivalves, and dead coral rubble contained abundant bivalves (Lithophaga aristata, Lithophage plunula, and Lithophaga attenuata; see Scott et al. 1988). Sponges were less obvious bioeroders in samples of reef substra tum from Champion Island than those we have observed in the Caribbean. Sipunculans also appeared to be relatively less impor tan t than polychaetes compared to observations made in the Caribbean (Moran and Reaka 1988, 1991; Reaka-Kudla , pers. obs.). In the retrieved experimental blocks, bivalves and worms were c o m m o n but sponges rarely were observed.

Bioerosion and encrustation on cathedral limestone (LS) blocks

After calcareous encrusters were removed from the blocks, it was clear that about 5% of the subst ra tum had been removed by bioeroders (Table 1). Total bioerosion (kgm -2 yr -1) did not vary significantly among frames (0.50 > p > 0.25) or depths (0.25 > p > 0.10, nested ANOVA, Sokal and Rohlf 1969). About 1% of each LS block's mass was added per year by the settlement of encrusting organ- isms (serpulid polychaetes, bryozoans, foraminiferans, coral- line algae, and epilithic bivalves, Table 2A). Of the total accretion, 14.3% (_+ 1.9 SE) was retrieved from the top, 31.0% (_+2 .5SE) f rom the sides, and 57.6% (_+ 3.6SE) from the bot toms of the blocks. Area-specific encrustat ion differed significantly among the upper, lateral and lower surfaces of the blocks from both shallow (Kruskal-Wallis [ K W ] test, p < 0.001) and deep (KW test, p < 0.001) habi-

Table 1. Carbonate lost from cathedral limestone (LS) blocks (after encrusting organisms were removed), mean _+ standard error, n = 33 in all cases

A. Total bioerosion % of block removed yr 1 4.6 + 0.2 kgm-2 yr -1 4.1 _+0.2 lm 2yr i 1.8_+0.1

B. Internal bioerosion % of block removed yr- 1 0.7 _+ 0.1 kgm-2yr -1 0.6_+0.1 lm 2yr 1 0.3-+0.03

C. External bioerosion % of block removed yr 1 3.9 _+ 0.2 kgm 2yr-~ 3.5_+0.2 lm 2yr 1 1.5_+0.1

Table 2. Encrustation by calcareous organisms on cathedral lime- stone (LS) blocks in shallow and deep habitats, mean_+ standard error, n = 18 for shallow and n = 15 for deep

A. Total accretion Habitat % added yr- 1 Shallow 0.9 ± 0.2

Deep 1.3 _+ 0.2 kg m 2 yr- 1 Shallow 0.6 _+ 0.1

Deep 1.0 + 0.1 lm 2 y r - 1 Shallow 0.3 +0.1

Deep 0.4 _+ 0.1

B. Area-specific encrustation (mg cm-2 yr- 1) Tops of blocks Shallow 7.0 ± 0.9

Deep 12.1 _+ 2.4 Sides of blocks Shallow 10.7 _+ 1.2

Deep 11.3 _+ 1.9 Bottoms of blocks Shallow 35.0 _+ 6.3

Deep 61.4 + 8.9

tats, with most accretion being on the bot toms of blocks (Table 2B). Encrustat ion on the tops and sides of blocks did not vary with depth (t' test, p > 0.05 in each case). However, settlement on the bo t toms of LS blocks was significantly greater in deep than shallow sites (t' test,

= 0.03).

Bioerosion of Porites lobata (PL) blocks

In contrast to the LS blocks (5% loss), the P L blocks lost about 61% of their mass and volume yr -1 during the experiment (Table 3A). There were no significant differen- ces in amount of P L bioerosion among frames (KW test, p > 0.05) or depths (f test, p = 0.48). Because of the differ- ence in density between P L and LS, the bioeroded volumes of the two types of substrata yield a better estimate of sediment produced than bioeroded masses. Whereas only about 2 1 y r - 1 of sediment was produced by bioerosion of the LS, about 24 l m - 2 y r -1 was removed from the PL.

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Table 3. Carbonate lost from Pori~es lobata (PL), mean ± standard error, n = 18

A. Total bioerosion % of block removed yr- 1 60.5 ± 5.4 kg m- z yr- ~ 25.4 _+ 2.4 lm-2yr -1 23.7+_2.3

B. Internal bioerosion % of block removed yr- 1 0.6 _+ 0.1 kgm-2yr 1 2.6_+0.1 lm 2yr-I 2.4_+0.1

C. External bioerosion % of block removed yr- ~ 59.9 _+ 5.4 kgm-2yr 1 22.8_+2.4 1 m-Zyr - 1 21.3 _+ 2.3

Internal versus external bioerosion

Following retrieval, live internal bioeroders, primarily worms and bivalves, were observed in all PL blocks and in all but one of the LS blocks. After only 14.8 months' exposure, a live bivalve 19 mm long was observed with its opening at the surface of a PL block, and the burrow of a bivalve 9 mm long was found in a LS block. Forty-five percent of the PL blocks and 50% of the LS blocks contained boring bivalves.

Both the PL and LS blocks sustained losses of about 1% yr 1 due to internal bioerosion (Tables 1B, 3B). For each square meter of substratum, internal bioeroders excavated 0.3-2.4 1 of LS or PL sediment per year, respect- ively.

By establishing the amount of internal bioerosion through computer digitization of holes in the slabbed blocks, the amount of external bioerosion could be cal- culated (total-internal = external bioerosion). External bi- oerosion removed from 4% to almost 60% of the volume and mass of LS and PL blocks (Tables 1C, 3C). Thus, for each square meter of substratum, external bioeroders pro- duced 1.5-21.3 1 of LS and PL sediment, respectively.

Using the initial heights of the PL and LS blocks and the proportion of sediment that was removed by external bioerosion from these substrata as a base for calculation, the average height of coral skeleton was reduced by 2.3 cm y r - 1 (2.3 m century- 1) and the average height of reef basement (comparable to the LS tested) was decreased by 0.2 cm yr - 1 (0.2 m century 1).

These data suggest that internal bioeroders may have been less affected by the hardness of the substratum than external bioeroders, and that external bioerosion is much more significant than internal bioerosion for breakdown of the reef framework on Champion Island.

Discussion

Several lines of evidence suggest that rates of bioerosion on reefs of the Galfipagos Islands are as high, or perhaps higher, than those measured in the present study. This experiment demonstrated that light porous skeletons of

Porites lobata (PL) suffer much higher rates of bioerosion (particularly external bioerosion) than harder, denser sub- strata such as cathedral limestone (LS). Although the LS did register moderate bioerosion (3-5% of mass and vol- ume yr-1) in comparison to the low rates found in some other regions (e.g., the mid-Pacific, Highsmith 1981), and although the reef pavement deposited by coralline algae and other organisms is hard and dense compared to the skeletons of most corals, our unquantified observations suggest that the carbonate reef pavement may be less resistant to bioerosion than the LS used in the experiments (pers. obs. MLRK). If so, bioerosion of the LS blocks would underestimate the amount of bioerosion occurring on many hard reef substrata at Champion Island.

Results from these LS blocks also estimate the magni- tude of carbonate deposition by encrusting organisms in this environment. More encrustation was found on the bottom than on the top and sides of the blocks, indicating either a preference for settling on dark undersides of reef structures by encrusting organisms and/or more extensive grazing and mortality of encrusters on the upper surfaces of reef substrata. Encrusters may settle disproportionately in deeper habitats, as evidenced by significantly higher accretion on the bottoms of blocks at l l - 1 3 m depth versus 5 - 6 m depth. Although small sea urchins occa- sionally excavate under blocks in experimental situations similar to ours, no excavations were observed on the bottoms of the LS blocks. The activities of micro-grazers also may influence the standing crop of encrustation, but we did not observe this activity. The scrapes on the blocks provided additional evidence that sea urchins and fishes were the predominant agents of external bioerosion. The LS blocks (which sustained relatively low external grazing) supported considerable encrustation, while the PL blocks (which suffered heavy losses due to scraping) were almost devoid of encrusters. If similar rates of settlement occurred on both, the extensive grazing on the PL blocks may have removed encrustation as fast as it formed. On substrata with moderate abundances of scapers or pickers, grazers may continually remove settling encrusters. Thus, if encrusters had not been abundant on the LS blocks, the rate of LS substratum removal might have been even higher than was measured, especially in the shallow environment that supported high urchin densities.

Bioerosion also may have been underestimated in this study because the three-dimensional topography of the reef made it difficult to place the rigid frames so that all points of the frame were in full contact with the surface of the reef. Two PL blocks with unusually low bioerosion (3.9% and 24.0% volume loss) were not in direct contact with the substratum, possibly limiting access by urchins. In addition, the study did not include the effects of large scale bioerosion, whereby external and internal bioeroders undercut and bore into reef structures, weakening the structure or its attachment so that storms and other disturbances topple coral colonies (Colgan 1990). A large (2m diameter) fragment of coral from the study site, with an iron reinforcing bar still imbedded, was observed at the bottom of the steep reef slope (24 m depth).

Despite the remarkable abundance and conspicuous- ness of boring lithophagid bivalves in live coral in the

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eastern Pacific in general and in the Galfipagos in parti- cular, the results of this study demonstrated the over- whelming importance of external bioerosion for the ob- servable decline of reef framework on the patch reef at Champion Island. Other studies have shown that the reefs of the Galfipagos Islands are in serious jeopardy. Up to 95-99% of the living coral in the Galfipagos Islands bleached and died following the 1982-1983 ENSO event, and has not been replaced by recruitment (Glynn 1984, 1990). In addition, the ENSO event of 1982-1983 preceded a redistribution and increase in local populations of E. thouarsii (from 5 individuals m-2 to 30 individuals m-2 before and after the 1982-1983 ENSO event) in shallow reef habitats of the Galfipagos Islands. Whereas Eucidaris was considered a major coral bioeroder in the Galfipagos Islands (Glynn et al. 1979; Glynn and Wellington 1983), in other regions, they appear to feed on filamentous or larger algae. When they became concentrated in shallow habitats in the Galfipagos Islands after the 1982-1983 ENSO event, they were capable of feeding on live coral (Glynn 1988b). The abundance of Eucidaris has remained high and, as observed in this study, they continue to feed on live coral. The fact that the PL blocks were reduced much more than the LS blocks suggests that Eucidaris and/or other grazers selectively graze on soft compared to hard substrata. Feeding preferences such as these have been demonstrated in several sea urchin species (Carpenter 1981; Shanula and Ndibalema 1986; Eakin 1988).

Our observations suggest a hypothesis for the prolifer- ation of E. thouarsii in shallow reef habitats after the 1982-1983 ENSO event in the Galitpagos Islands. When the lithophagid bivalves inhabiting live coral die, coral regenerates over perforations in the surface. If a high proportion of the corals and bivalves die (Glynn 1988a; 1990; Scott et al. 1988), numerous openings of the boring bivalves are not closed by coral growth. Following the 1982-1983 ENSO event, benthic algae became more abundant and grazing by fishes and E. thouarsii enlarged the external openings of the boring bivalves on the surface of the coral. We propose that E. thouarsii, much like Acanthaster planci, recruit into the cryptic holes and spaces of the reef (Birkeland 1982). Dissection of coral skeleton and other field observations confirmed that ju- venile Eucidaris did inhabit the empty holes left by lithophagid bivalves. The sudden increase in available holes made by the eroded surface of the dead corals would have provided increased habitat for settling E. thouarsii larvae. Post-E1 Nifio increases in crustose coralline algae (CCA) cover (Eakin 1992), combined with the relatively high nutritional value of CCA (Hawkins 1981), also could have contributed to increased echinoid recruitment and survival. When the juveniles outgrew their cryptic crevices (including the vacant boreholes of lithophagid bivalves), they would have emerged onto the local reef in large numbers. While more quantitative observations and experiments are necessary to confirm or refute this hypoth- esis, we suggest that vacant holes of lithophagids on a mostly dead reef may have contributed to the recruit- ment of Eucidaris and hence induced a positive feedback in the cycle of erosion that followed the 1982 1983 ENSO event.

The results of our experiments confirm visual observa- tions that the rate of bioerosion on the reef at Champion Island is high and is causing rapid destruction of the reef framework. The volume of PL blocks was reduced by 61% per year and the mass of coral sediment removed was approximately 25 kg m-2 yr - 1. In bucket experiments conducted for several days, Glynn (1988b, 1990) measured even higher rates of bioerosion at other sites in the GalS, pagos Islands and reported that 20-45 kg of sediment m -2 yr - 1 was removed (E. thouarsii were responsible for 67-75% of this erosion). These rates, as well as those reported for Champion Island in the present study, indi- cate that bioerosion removes more coral skeleton than is produced in the Gal/tpagos Islands (net community pro- duction of 8 - 1 6 k g m - Z y r 1, Glynn 1988b), and easily could cause the rapid changes in topography that we observed on the reef at Champion Island. Similar rates of post-El Nifio bioerosion were reported by Scott et al. (1988) for Costa Rican reefs; however, internal bioerosion was more significant there. Overall, while the results are conservative, it is clear that bioerosion of coral reefs in the Galfipagos Islands is producing serious declines in carbon- ate frameworks. If such losses continue unabated, coral reefs could be eliminated from the Gal@agos Islands entirely.

Acknowledgments. This study was funded by two National Science Foundation grants, OCE-8716726 and OCE-9018392 to PWG, and funds from the Dean, College of Life Sciences, University of Maryland to MLRK. We gratefully acknowledge the field assistance of Godfrey Merlen, Michael Moore and Fernando Rivera, and the laboratory assistance of Valerie Cappola, Sybille Cooper and Jennifer Gavin. Field work in the Gal@agos Islands was made possible by permission of the Gal/tpagos National Park Service, and logistical support was provided by the Charles Darwin Research Station and Charles Darwin Foundation. Transportation of equip- ment and personnel was subsidized by American Airlines, USA, and Transporte Aerea Militar de Ecuador (TAME) airlines, Ecuador.

References

Birkeland C (1982) Terrestrial runoff as a cause of outbreaks of Acanthaster planci (Echinodermata: Asteroidea). Mar Biol 69: 175 185

Carpenter RC (1981) Grazing by Diadema antillarum (Philippi) and its effects on the benthic algal community. J Mar Res 39:749-765

Colgan MW (1990) E1 Nifio and the history of eastern Pacific reef building. In: Glynn PW (ed) Global ecological consequences of the 1982-1983 E1 Nifio-Southern Oscillation. Elsevier, Amsterdam, pp 183-229

Eakin CM (1988) Avoidance of damselfish lawns by the sea urchin Diadema mexicanum at Uva Island, Panama. Proc 6th Int Coral ReefSymp 2:21 26

Eakin CM (1992) Post-E1 Nifio Panamanian reefs: less accretion, more erosion and damselfish protection. Proc 7th Int Coral Reef Symp 1:387-396

Glynn PW (1984) Widespread coral mortality and the 1982/83 E1 Nifio warming event. Environ Conserv 11:133-146

Glynn PW (1988a) E1 Nifio-Southern Oscillation 1982 1983: Near- shore population, community, and ecosystem responses. Ann Rev Ecol Syst 19:309-345

Glynn PW (1988b) E1 Nifio warming, coral mortality and reef framework destruction by echinoid bioerosion in the eastern Pacific. Galaxea 7:129 160

Glynn PW (1990) Coral mortality and disturbance to coral reefs in the tropical eastern Pacific. In: Glynn PW (ed) Global ecological consequences of the 1982 1983 E1 Nifio-Southern Oscillation. Elsevier, Amsterdam, pp 55-126

Glynn PW (1994) State of coral reefs in the Gal~tpagos Islands: Natural versus anthropogenic impacts. Mar Poll Bul129 :131 140

Glynn PW, Wellington GM (1983) Corals and Coral Reefs of the Gal~pagos Islands. University of California Press, Berkeley, 330 pp

Glynn PW, Wellington GM, Birkeland C (1979) Coral reef growth in the Galfipagos: Limitation by sea urchins. Science 203:47 49

Guzm~n HM, Cortas J (1989) Coral reef community structure at Carlo Island, Pacific Costa Rica. PSZNI: Mar Ecol 10:23-41

Hawkins CM (1981) Efficiency of organic matler absorption by the tropical echinoid Diaderna antillarum Philippi fed non-macro- phytic algae. J Exp Mar Biol Eco149:245 253

Highsmith RC (1981) Coral bioerosion at Enewetak: agents and dynamics. Int Revue Ges Hydrobio166:335 375

Hutchings PA (1986) Biological destruction of coral reefs. Coral Reefs 4:239 252

Hutchings PA, Kiene WE, Cunningham RB, Donnelly C (1992) Spatial and temporal patterns of non-colonial boring organisms (polychaetes, sipunculans and bivalve molluscs) in Porites at Lizard Island, Great Barrier Reef. Coral Reefs 11:23-32

Jokiel PL (1986) Growth of the reef coral Porites compressa on the Coconut Island reef, Kaneohe Bay. In: Jokiel PL, Richmond RH, Rogers RA (eds) Coral reef population biology. Hawaii Inst Mar Biol Tech Rpt 37, pp 101 110

Kiene WE (1988) A model of bioerosion on the Great Barrier Reef. Proc 6th Int Coral Reef Symp 3:449 454

Klein C, Hurlbut CS (1977) Manual of mineralogy (after James D.Dana), 20th ed. John Wiley and Sons, New York, pp. 202- 203

Macintyre IG (1984) Preburial and shallow-su~surface alteration of modern scleractinian corals. In: Oliver WA Jr, Sando WJ, Cairns SD, Coates AG, Macintyre IG, Bayer FM, Sorauf JE (eds) Recent advances in the paleobiology and geology of the Cnidaria. Palae- ontogr Amer 54:229-244

Macintyre IG, Glynn PW, Cort6s J (1992) Holocene reef history in the eastern Pacific: Mainland Costa Rica, Carlo Island, Cocos

107

Island, and Gal/tpagos Islands. Proc 7th Int Coral Reef Symp 2:1174 1184

Moran DP, Reaka ML (1988) Bioerosion and the availability of shelter for benthic reef organisms. Mar Ecol Progr Ser 44:249- 263

Moran DP, Reaka-Kudla ML (1991) Effects of disturbance: disrup- tion and enhancement of coral reef cryptofaunal populations by hurricanes. Coral Reefs 9:215-224

Risk MJ, MacGeachy JK (1978) Aspects of bioerosion of modern Caribbean reefs. Rev Biol Trop 26:85-105

Robinson G (1985) Influence of the 1982-1983 E1 Nifio on Galfipagos marine life. In: Robinson G, del Pifio EM (eds) El Nifio in the Gal/tpagos Islands, Charles Darwin Foundation for the Gal/tpagos Islands, Quito, Ecuador, pp 153-190

Rose CS, Risk MJ (1985) Increase in Cliona deIitrix infestation of Momasrrea cavernosa heads on an organically polluted portion of the Grand Cayman fringing reef. Mar Ecol 6:345-363

Scott PJB, Risk MJ (1988) The effect of Lithophaga (Bivalvia: Mytilidae) boreholes on the strength of the coral Porites lobata. Coral Reefs 7:145-151

Scott PJB, Risk MJ, Carriquiry JD (1988) E1 Nifio, bioerosion, and the survival of east Pacific Reefs. Proc 6th Int Coral Reef Symp 2:517-520

Shanula JP, Ndibalema V (1986) Grazing Preferences of Diadema setosum and Heliocidaris erythrogramma (echinoderms) on an assortment of marine algae. Aquat Bot 25:91-95

Sokal RR, Rohlf FJ (1969) Biometry. 2nd edition. WH Freeman and Co, San Francisco, 859 pp

Trudgill ST (1983) Measurements of rates of erosion of reefs and reef limestones. In: Barnes DJ (ed) Perspectives on coral reefs. Brian Clouston Pub, Manuka, pp 256-262

Woodley JD0 Chornesky EA, Clifford PA, Jackson JBC, Kaubman LS, Knowlton NK, Lang J, Pearson MP, Porter JW, Rooney MC, Rylaarsdam KW, Tunnicliffe VJ, Wahle CM, Wulff JL, Curtis ASG, Dallmeyer MD, Jupp BP, Koehl MAR, Neigel J, Sides EM (1981) Hurricane Allen's impact on Jamaican coral reefs. Science 214:749-755

Zar JH (1984) Biostatisticat analysis. Prentice-Hall, New Jersey, 718 PP

Note added in proof

For a report on bioerosion and reef carbonate budgets in Panama, please see Eakin (this volume). Eakin CM (1996) Where have all the carbonates gone? A model comparison of calcium carbonate budgets before and after the 1982 1983 E1 Nifio at Uva Island in the eastern Pacific. Coral Reefs 15:109 119