III 'LLETIN OF MARINE SCIENCE. 33( I): 132-151. 1983 PAPER

CARIBBEAN STAG HORN CORAL POPULATIONS: PRE-HURRICANE ALLEN CONDITIONS IN DISCOVERY BAY,

Verena TunniclifJe

ABSTRACT In August 1980, Hurricane Allen caused damage of catastrophic proportions on the coral reefs of Discovery Bay, Jamaica. The extensive staghom coral (Acropora cervicornis) beds were flattened and rapid recovery is not evident. This study describes the staghom populations as they were before the hurricane; work on the present state of the reefs is in progress. Three areas of Discovery Bay were studied. A. cervicornis was most abundant on the haystacks of the west fore reef between 5 and 20 m depth where up to II corals per m2 produced a maximum of 10 m of branches. Here the individual corals were significantly larger than those of the east fore reef or the back reef. Although a significant negative cor-

relation of growth rate with depth (cm 'yr 1 = 14.46 - 0.19 [depth, m]) was found on the west fore reef, the shallow corals were not taller but rather showed a higher level of branching; there is an indication that shallow corals branched more frequently. Contacts between adjacent corals were common and showed varying grades of tissue acceptance. The num ber of between- coral grafts did not correlate significantly with population density but did with water depth. An examination of branch orientation across the fore reef revealed a shift coincident with wave refraction but scatter was very high; frequent breakage disrupts the preferred growth directions. Most of the staghoms at all sites had been broken at some time but the predominant method of reattachment differed at each site. The numbers of broken branches in corals on the fore reef was a function of coral size; in the back reef they were directly proportional to depth which suggests a lagoonward transport of the corals. An average of one-third of each coral is bare of tissue. The major predators are a sea urchin, damselfish, a snail and a polychaete. Clionid sponges are abundant in the coral skeleton. There is a large contribution by A. cervicornis to the skeletal calcium carbonate of the reef, and thus to vertical reef accumulation; this study estimates 1.4 kg·m-2·yr-1 in the cervicornis zone. There appeared to be a slight down-reef shift of material before it was cemented in place. A. cervicornis dominated the west fore reef community; abundances of massive corals fell where those of the staghom rose. The success of A. cervicornis derived primarily from its ability to regenerate from fragments. It exerts a competitive dominance over other space-occupiers by virtue of its high growth rate, a pronounced shading effect, mechanical damage to underlying corals through its break- age, and aseasonal recruitment to available spaces by fragmentation. There does appear to be a limit on its tolerance to disruption; present questions center around the fate of these Jamaican reefs.

Many reefs of the are dominated by monotypic stands of the staghorn coral Acropora cervicornis (Lamarck). Dense "bramble-patches" of this branching stony coral can be found in the protected waters of the Caribbean: Jamaica (Go- reau, 1959), Florida (Shinn, 1976), Bahamas (Bottjer, 1980), (Almy and Carrion-Torres, 1963) and (Kuhlman, 1974) among others, and it is present as scattered stands in more exposed areas such as those of the Dutch Antilles (Roos, 1971), St. Croix (Rogers, 1979) and (Lewis, 1960). As one of three species of Acropora in the Caribbean, it occupies the most extensive depth ranges from 0 to 30 m. In August 1980, Hurricane Allen passed very close to the reefs of the northern shore of Jamaica. The resulting damage to the reef was catastrophic in proportions

132 TUNNICLIFFE: CARIBBEAN STAG HORN CORALS 133

Figure I. Map of Discovery Bay, Jamaica. The three study areas are marked with dashed lines.

(Woodley, 1980; Porter et aI., 1981; Woodley et aI., 1981) and the fields of A. cervicornis were flattened; mortality of this coral during and after the hurricane was over 95% (Knowlton et aI., 1981). An extensive research effort to determine the patterns of recovery of these reefs is presently centered at the Discovery Bay Marine Laboratory in Jamaica. The study reported here was conducted during the 3 years prior to the hurricane. It represents an intensive investigation of A. cervicornis beds that no longer exist. These results may be useful, however, (1) as an example of the dynamics of similar assemblages in other areas, and (2) to compare with the recovery sequence now taking place on the Discovery Bay reefs. Much of this study was conducted with the view to understanding the effects of waves on both coral and community biology. Mechanical and hydrodynamic features of A. cervicornis are described in TunnicIiffe (1979) and (1982) while the effects of wave breakage on reproduction are outlined in Gilmore and Hall (1976) and Tunnicliffe (1981).

Study Area

Discovery Bay is located on the north shore of Jamaica in the Caribbean (Fig. I). The mouth of the bay is blocked by well-developed reefs but an entrance channel was dredged to a depth of 13 m. The reef structure and communities of this area have been extensively described by Goreau (1959), Goreau and Goreau (1973), Kinzie (1973) and Goreau and Land (1974) among others. The main study areas for this work are indicated on Figure I: Pinnacle Two on the west fore reef, Damsel Gardens in the east back reef and discrete sites on the east fore reef. Supplementary information was added from adjacent areas. Pinnacle Two is a large "haystack" (Kinzie, 1973) extending unbroken from the cresting reef top to 30 m in depth and is about 300 m long and 100 m wide. It is bounded by two deep sand channels on either side and a sandy moat at 30 m separates this haystack from a large seaward mound ("the pinnacle") that rises to 23 m and then drops away steeply to the deep fore reef (Fig. 2). The biological zonation follows that described by Goreau and Goreau (1973): reef crest zone dominated by Acropora palma/a, a mixed zone of many coral species, the cervicornis zone and the deep fore reef where plating corals are common. The coral population lagoonward of the reef crest is sparse and dominated by mound corals. A poorly sorted sediment covers the bottom and frequent resuspension of this sediment results in high turbidity (Dodge et aI., 1974). The bottom slopes down into a deep lagoonal basin 150 m behind the reef crest in which no corals grow. The east fore reef of Discovery Bay is an extensive plateau of low slope. Topographically, the area 134 IlULLETIN OF MARINE SCIENCE. VOL. 3J. NO. I. 19~3

Figure 2. Sketch of Pinnacle Two, west fore reef. This haystack supported prolific A. cervicornis growth on the terrace. It is about 350 m from reef crest to the top of the pinnacle where water depth is 23 m. A. reef crest-palmata zone 2 m; B, mixed zone 7 m; C, cen'icornis zone, 15 111; D, sand channel and moat, 30 m and E, pinnacle, 25 m. has few of the distinctive haystack-sand channel structures of the west side. Organism zonation is indistinct; sponges, gorgon ian corals and mound corals predominate and acroporid corals are less common (Liddell and Ohlhorst, 1981).

METHODS

On each of the study areas, a line transect was established for study of individual A. cervicornis corals. On Pinnacle Two, this transect extended from the reef crest to 30 m in depth for a total of 280 m downslope. A compass was used to maintain a heading of N30oE, the direction in which the haystack extends from the reef crest. The transect in the back reef traversed 120 m perpendicular to the reef crest from 3 to 13 m in depth, below which the sand bottom was unpopulated. Because of the large distance on the east fore reef from the reef crest to 30 m in depth, 50-m transects with N300E orientations were studied at depths of6 m, 9 m, 12.5 m, 15.3 m, 21.5 m and 26 m. I estimated the population densities of A. cervicornis in two ways: the number of corals per square meter and the total length of live branches of A. cervicornis. Every 10 m from the reef crest, a 4-m' quadrat divided into I-m square areas was placed on the reef; measurements in each I-m' partition were taken with a tape measure and the four measures were averaged. Because of the tendency of A. cervicornis to intergrow and fragment, it is occasionally difficult to identify a single coral. Nearly all structures of this colonial animal could be recognized by a single basal stalk from which all subsequent branches formed. The A. cervicornis that was under the mark at each meter along the transects was examined for a number of variables. For the corals along the Pinnacle Two (n = 187) and back reef(n = 56) transects, these variables were: maximum height above substratum, maximum branch spread (width), highest branching order, basal circumference, estimated amount dead, the number of grafts formed (within the coral and to others), numbers of tip, branch and basal fractures, type of basal attachment and, lastly, the presence and type of predation. The east fore reef corals (n = 128) were examined only for height, width, amount dead, total number offractures, basal attachment and predation. The variable "branching order" was determined by the method of Strahler (1957). The end branches are of order TUNNICLIFFE: CARIBBEAN STAGHORN CORALS 135

A.

0

1000 CJ ~ CD E U 3~ 000 -'0 :;: 0- 3 c: 600 ...J'" ~ -20 u ~OO c: 0 cD 200

~ .,...... ,.-,- -30 20 40 60 80 100 120 140 160 180 200 220 240 260 280

Distance from reef crest (m)

B. c.

Ne 600 E 400 400 u - 1\ ~: 2.00 /'... / -GI\t,o I , I 'I I I I t 2.0 40 60 eo 100 120 10 20 Distance (m) Depth (m) Figure 3. Distribution of Acropora cervicornis. The abundances of staghom coral are overlaid on the reef profile on (A) the Pinnacle Two transect and (B) the back reef transect. Distribution is plotted against depth for (C) the east fore reef where the coral was measured discontinuously.

I, two (or more) order I branches join to form an order 2 and so on. The data sets for each of the measured characteristics were tested for normal distributions (Zar, 1974) and non-parametric tests were used where appropriate. When A. cervicornis branches grow close together, they may veer away or fuse. These grafts were classified as "autografts" (within one coral) or "allografts" (between separate corals). When the 4-m2 quadrats were placed on the reef, they were photographed. The pictures were replicated four times from October 1977 to April 1979. The growth of individual staghom corals could be traced and for each identifiable coral the interval in which branching occurred was noted. These photographs were also used to study the orientation of A. cervicornis branches. The 100 longest branches in each quadrat on the Pinnacle Two transect were measured for length and orientation. During the months of April and May 1978, corals were stained with alizarin red, a dye that is readily incorporated in the matrix of the skeleton (see Dustan, 1975, for methodology). The calcium carbonate deposited in the 8-h staining period included the dye giving the outer skeleton a uniform pink color; subsequent growth remained white. These corals were collected II months later, the tissue removed and the linear extensions of all the branches measured. Density of the new growth was also measured to detect any changes with depth. I estimated the amount of bare skeleton on each coral and recorded the frequency of injury by the four major predators of A. cervicornis. The amount of dead branch material lying on the substratum and the extent ofthe territorial "lawns" of damselfish in the A. cervicornis branches could be estimated on the photographs; in areas of high staghom density additional photographs of l_m2 areas augmented the accuracy of the estimates. The state and extent of the lawns on the Pinnacle Two transect were recorded in August 1978 and compared to the preceding and succeeding pictorial records. The distributions of some other reef corals were examined also. The massive coral Montastrea annularis is important as a framework builder in some of the reef zones (Goreau, 1959; Goreau and Land, 1974; Dustan, 1975). Abundances were recorded in the 4-m2 photograph by planimetric mea- surement. Porites aSlreoides is a small-polyped coral that forms low, massive and partially encrusting colonies. Colpophyllia natans, a meandrine coral, can form large heads over 1.5 m in height. The 136 BULLETIN OF MARINE SCIENCE, VOL 33, NO.1. 1983

Figure 4, A. The "mixed" zone at 6 m, The large mounds are Montastrea annu/aris, B. The "cer- vicornis" zone at 9 m. C. The back reef. At 8 m A, cervicornis lodges in the sand and much of the basal portion of the coral is dead, The apical polyps of the branch tips are evident and three urchins, Diaderna antillarurn can be seen, D. Broken A, cervicornis branches on a massive coral. The underlying Siderastrea siderea shows patches of abraded skeleton, The black mottling on many of the cervicornis branches indicates the presence of the sponge Chona aprica, maximum dimensions of these two corals were measured underwater along the transects: the former in a 2-m wide strip and the latter in a 4-m wide strip, For comparison with the other corals, their mean coverages for each IO-m long interval were used,

RESULTS Distributions The top 5 m (in depth) of the Pinnacle Two transect were dominated by Acropora palmata, A. cervicornis appeared abruptly 60 m from the crest (Fig. 3a). There were some, albeit very few, transitional forms that might have been A. prolifera; as it was difficult to distinguish this species here (Tunnicliffe, 1980a) all forms were treated as A. cervicornis. In the mixed zone (Fig. 4a) numerous species of corals appeared and cover by A. cervicornis was correspondingly variable. The "cervicornis" zone proper began at about 150 m from the reef crest; cover increased to over 10 m of live branches per square meter (Fig. 3a). On the fore reef terrace at about 14-m depth, the staghom populations-and those of other corals-appeared to be reduced by the fish pots thrown onto the reef (Woodley, 1979). On the steep slope into the moat (240 m from the crest) A. cervicornis density dropped rapidly and fell to zero in the sand. Although the pinnacle rises up again to 23 m there were less than a dozen staghom corals on the entire structure. The results from counting the number of corals per m2 on this transect showed the same trends as the length measurements; a correlation analysis of number of corals with extent of live branches (Fig. 3) gave a Pearson correlation Tl'NNICl.lFFE: CARlIIllEAN STAGHORN CORALS 137

30

;-!20 Q; 50 >- 0 u c: Z ., lIJ :2 :> 0 40 o .E lIJ ., If 0 .g 30 0 •• 5 10- a'" 20 ~., 0c: 10 0 r---1 ~" 20' • '40 • , • 6b • eO .2 .4 .6 .8 1.0 CORAL t£IGHT (cm.> Weight (gm/cm)

Figure 5. (Left) Histogram of A. cervicornis height distribution. The absence of small corals is marked although heights were measured in a number of seasons. Measurements are for Pinnacle Two transect only. Figure 6. (Right) Weight of new coral growth as a function of ambient light levels. Light as a function of depth on the fore reef(e) and the back reef(Q) was determined using the equations of Brakel (1976) for these areas. The weight is that of the new coral tips formed in a year's growth. coefficient of r = 0.80 (n = 21; P < .00 I). In the area of greatest cover, mean value of the 4-m2 quadrat was 11.0 corals/m2• Figure 3b represents the cover of A. cervicornis in the back reef where maximum densities were only 400 cm/m2• In shallow water, A. palamala of the rear zone predominated, and below 2 m the massive corals were common. The substratum was mostly unconsolidated and covered with sediment (Fig. 4c); the population peak 80 m behind the reef crest was due largely to a mound of rubble on which the corals gained purchase. Beyond 90 m from the crest A. cervicornis was the only coral to be found lying loosely in the sand to a depth of 13 m. No epibenthic fauna was found beyond this point. The distribution of A. cervicornis where measured on the east fore reef (Fig. 3c) differed greatly from that of the west side. There were patches ofthe coral scattered about the platform; cover was greatest at the IS-m site (230 cm/m2). Channel dredging may have adversely affected these corals as seen in Barbados (Dodge and Vaisnys, 1977).

Coral Meristics The only non-normal height distribution was that of the east fore reef population where small acroporids of dubious identification weighted the lower end. Figure 5 shows the height distribution of the staghorn of the Pinnacle Two transect- very few small or "juvenile" corals were encountered. A summary of the mea- surements made on all the corals can be found in Table 1. (A detailed list is presented in Tunnicliffe, 1980b). As would be expected, there were high corre- lations between height and width (P < .001), height and branching (P < .01), height and circumference (P < .001), width and branching (P < .00 I) and width and circumference (P < .001); all are measures of the age ofthe structure. Crowd- ing in organisms that need light may cause them to grow taller at the expense of 138 llULLETIN OF MARINE SCIENCE. VOL 33. NO. I. 1983

Table I. Dimensional measurements (in cm) for Acropora cervicornis on the three study areas of Discovery Bay (% dead refers to the estimated amount of each coral not covered by live tissue)

Range Standard Mean Deviation Minimum Maximum Sample Size Pinnacle Two Height 38.9 14.9 5.0 85.0 187 Width 61.3 24.0 4.0 130.0 187 Circumference 6.4 1.7 2.0 12.0 170 Branching 4.8 1.3 1.0 9.0 186 % dead 35.9 26.3 0 95.0 187 Back Reef Height 27.4 12.8 7.0 70.0 56 Width 48.9 23.9 13.5 115.0 56 Circumference 6.4 1.7 2.5 10.0 55 Branching 3.1 1.0 2.0 6.0 56 % dead 35.1 28.2 0 90.0 56 East Fore Reef Height 27.2 18.5 1.0 80.5 126 Width 47.2 26.2 1.0 109.0 127 % dead 31.8 29.3 0 90.0 125

lateral extensions. However, non-parametric correlations of coral height with population density revealed no significant relationships. A. cervicornis height and width on Pinnacle Two were significantly larger than those of both the back reef and the east fore reef (all t-tests P < .001, separate variance). Level of branching was also higher on Pinnacle Two than the back reef (P < .001, pooled variance) although the circumference of the corals of the two populations was not significantly different (Table I). Because these measurements were made with the hydrodynamic stability of the corals in mind, water depth was examined as a possible factor influencing coral dimensions. The hypothesis that shallow corals were shorter to reduce drag was rejected as there was no significant correlation between depth and coral height or width. However, despite higher growth rates in the shallow corals (see below) they were not taller than those deeper. Indeed, for the Pinnacle Two transect, there was a significant negative correlation (at P < .05) between depth and branching level: shallow corals appeared to branch more frequently.

Branching Time It became apparent during this study that A. cervicornis branched about once a year. Field and photographic observations indicated branching occurred in the shallowest corals during the months of January and February but later in deeper water. To quantify this impression the lengths of a sample ofthe youngest branches were measured; the longer these branches, the greater the time since branching. Ten to 20 branches were used in 10 corals, at 18 depth-stations in April 1979. A simple correlation showed a significant decrease in mean tip length (r = 0.79; n = 15) from 4.1 cm at 6.1 m to 0.4 cm at 15.6 m (a discrepancy not explained by differential growth rates). At this time, the lengths ofthe youngest branches at the lowest four stations indicated they had not bifurcated since the preceding year (x = 10.0 cm, 16.6 m depth). TliNNICLIFFE: CARIIJIJEAN STACiHORN CORALS 139

'00 M 60 I...---l ...en ~ ~ ~ 40 ci z

20

5.0 10.0 15.0 2QO 25.0 300

DEPTH (mJ

Figure 7. (Left) Grafts formed between A. cervicornis colonies. The frequency of grafts appears to be a function of depth (r = 0.79). Figure 8. (Right) Branch orientation on Pinnacle Two. Rosettes were made from 100 branch vectors at each station and plotted on a contour map of the reef. The deepest station may be responding to a long-shorc current while there is a tendency for the terrace corals to shift from a NE-SW to a N-S orientation as the water shallows. Depth values are accurate for the transect and the bordering sand channels; adjoining contours are estimates.

Grafts Two types of fusions between adjacent corals were observed. In the first, one branch is obviously dominant and may expand for a number of centimeters over the subordinate branch. J. C. Lang (pers. comm.) cal1s this interaction "simple overgrowth"; a similar phenomenon in Pacific acroporids is called "overgrowth." The second fusion is a complex interaction or a 'filling reaction' (Potts, 1976); branches contact and the suture zone is emphasized by swollen, bleached edges with a few smal1 corallites. This bond is not strong and may remain static over many months with no obvious dominant. At high population densities, there should be a higher probability that corals will intergrow and form grafts. However, a non-parametric correlation test be- tween population densities and number of al10grafts was not significant. Figure 7 presents a plot of number of allografts with depth (the correlation with autografts was insignificant). Greater graft frequency in shal10w water may be due to increased breakage there or to higher growth rates that increase the chances of contact.

Branch Orientation Chamberlain and Graus (1975) class A. cervicornis as a "high porosity" struc- ture; water flows through easily and leading branches provide little protection for posterior ones. A growth form that orients with respect to wave surge would reduce both form drag and the chance of breakage (Graus et aI., 1977). 140 BULLETIN OF MARINE SCIENCE. VOL JJ. NO. I. 19SJ

Table 2. Growth rates from 19 colonies of Acropora cervicornis in Discovery Bay; light values from Brakel, 1976

Light Depth (% surface No. (m) incidence) branches x cm/yr glem Mean g/yr Back Reef 7.3 37.0 6 14.1 .90 12.7 7.8 34.9 II 12.6 .85 10.7 8.3 33.0 2 10.0 .68 6.8 9.5 29.1 7 11.2 .66 7.4 11.5 23.5 6 7.4 .71 5.3 Fore Reef 5.5 48.0 11 10.9 .75 8.2 5.7 48.0 4 15.9 .93 14.8 7.2 43.5 5 11.9 .95 11.3 12.9 31.0 6 13.4 .79 10.5 13.0 30.8 5 14.0 14.1 28.6 4 12.6 .74 9.3 14.4 28.5 7 12.0 .71 8.5 15.8 25.8 2 8.0 .61 4.9 15.8 25.8 18 12.0 .62 7.5 27.4 13.0 10 9.2 .44 5.4 27.4 13.0 5 9.5 .32 4.7 27.4 13.0 8 14.8 .46 6.5 Pinnacle 21.4 18.6 3 3.5 .59 1.1 21.4 18.6 5 5.2 .49 2.4

Figure 8 represents the results of the orientation measurements on a contour map of Pinnacle Two reef. Observations at monthly intervals throughout 1977 and 1978 indicated the waves came from N35°E to N70oE. The orientation rosettes do not show the marked bimodality with wave direction of those recorded by Graus et a1. (1977) for A. palmata branches in St. Croix. Each station did show preferred growth directions although scatter was great and adjacent stations did not always correspond. It appears that trends of wave refraction over the reef (observed here and recorded in Grand Cayman by Roberts, 1974) are reflected in the dominant direction of growth: the approaching wave front assumes a more northerly direction as the reef shallows.

Growth Rates Growth information on each of 19 corals is listed in Table 2. Although the corals chosen for staining were small, some added over a meter of new branches in 11 months. Some individual branches grew at rates over 20 cm/yr. The mean growth rate of the 13 shallower corals of the fore and back reef areas where incident light exceeds 25% of surface levels (Brakel, 1976) is 12.0 cm/yr (s = 2.0; 88 branches). The mean annual weight increment per branch was 9.4 g (s = 2.8). The corals with the highest growth rates were the shallowest ones; it was not the deepest ones that grew slowest, but rather those corals on the pinnacle at the bottom of the fore reef transect (Fig. 2). Apart from the corals on this pinnacle, l the following equations describe the growth: fore reef: Rate (em ·ye ) = 14.46 - l 0.19 (depth in m); back reef: Rate (cm·ye ) = 23.18 - 1.37 (depth in m). Figure 6 is a plot of coral mean weight per unit length and available light. The variable light calculated by the equations of Brakel (1976) was used because of the effects of light on the calcification process (Goreau, 1963). The result shows that deeper corals were generally thinner and lighter. There was no significant change in coral density with depth-only in the actual TliNNICLIFFE: CARIBBEAN STAGHORN CORALS 141

Table 3. Frequencies of basal breakage of A. cervicornis within the three study sites. Basal condition is significantly different in each site; chi-square = 70 (P < 0.001,4 d.f.)

Row Total Pinnacle Two Back Reef East Fore Reef (N) Unbroken 12.8 16.4 38.1 84 Broken, uncemented 16.0 52.7 26.2 92 Broken, recemented 71.2 30.9 35.7 193 Column total (N) 187.0 55.0 126.0 368 branch thickness. There was, however, a substantial difference between the den- sities of new growth (x = 1.2 glcm3; s = 0.2; n = 15) and the older skeleton; the densities of stems of 11 corals had a mean of 2.48 glcm3 (s = 0.19). A light framework is first deposited to be filled in later. The density of pure aragonite is 2.95 glcm3 so the porosity of the older A. cervicornis stems is very low. Coral Breakage Much of the information on breakage and basal attachment of A. cervicornis has been reported previously (Tunnicliffe, 1979; 1981). Seventy-eight percent of the corals at all sites had been broken basally at some time; of these, 68% had been recemented to the reef by one of two mechanisms: the coral itself overgrew and reattached to the substratum or the dead basal area of the coral was recemented after settlement of either coralline algae or the benthic foram Gypsina plana Carter. Table 3 presents the frequency of broken corals at each study area. The chi-square analysis indicates that the frequency of unbroken, loose and recemented coral was significantly different among the sites (P «: .001). When the total number of fractures was examined-branches and tips includ- ed-coral sizes on the fore reef were the significant predictors of breakage: width (Pearson r = 0.23; P < .001), branching (r = 0.22; P = .001), and circumference (r = 0.24; P = .001). In the back reef, however, it was depth (and therefore distance away from the crest) that was significant (r = 0.57; n = 56; P = .001).

Coral Mortality Most A. cervicornis had bared skeletons at their bases with a receding tissue line; it was difficult to find a coral with all tissue present-particularly over 20 cm in height. The figures estimated for amount of each coral that was dead (Table 1) appear to be reasonable in that there is a good correlation with two variables that are function of the age of the present structure: height (P < .002) and width (P < .001) (non-parametric tests on n = 187 on Pinnacle Two reef). Depth was an insignificant factor. The older a structure was, the more likely it was to su'stain

Table 4. Frequency of predation on A. cervicornis by different organisms (data from corals on study transects). Numbers represent incidences of attack not total damage sustained

Damselfish Diadema Coralliophila Hermodice TOlal

Pinnacle Two 6% 8% 4% 18% (n = 187) East Fore Reef 13% 2% 5% 2% 21% (n = 128) Damsel Gardens 32% 2% 2% 36% (n = 56) Subtotal 13% 5% 4% '12%

Total corals afflicted (n = 371) 22112% 142 BULLETIN OF MARINE SCIEI'CE. VOL. JJ. :-;0. I. 1'laJ

'000

N E ~ '00

lQOO

] aoo

.<= g.600 --''" -5400 c P oslr~~s ~ 200

it>0 200 "0 "0 100 I I 150' , , , 2'00' , , '250 Distance from reef crest (m) rjrC-:>0_ ~ 100 1'0 200 2'0 OiSlonce Irom reel ernl Iml

Figure 9. (Left) Distribution of dead (--) and live (- - - -) staghorn branches on Pinnacle Two. The abundance patterns of the latter appear to be offset from the former by about 10m. Figure 10. (Right) Distributions of the major scleractinians of Pinnacle Two. The mixed zone, wherc they are most common extends from about 100 to 150 m from the crest; deeper the "cervicornis" zone starts. injury and predation resulting in partial colony mortality. However, in the back reef, depth was again the only significant variable (P < .001). T-tests (data normally distributed) for differences in amount dead among the three sites were not significant (which is not to say the sources of mortality were the same). Overall, much of the staghorn coral was dead (Table I). These extensive dead surfaces provided substrata for the settlement of many other organisms such as coralline algae, forams, bryozoans and sponges. The four most important predators of A. cervicornis were the echinoid Diadema antillarum. the gastropod Coralliophila sp., the polychaete Hermodice caruncu/ata and the three-spot damsel fish Eupomacentrus p/anifrons. Diadema removed large areas of tissue, scraping the underlying eorallites and frequently leaving the star- shaped impressions of the jaws. Damselfish tended to remove bite-sized patches oftissue while also damaging the underlying skeletal structure. Hermodice ingested the entire tip of a branch, digested the tissue and withdrew leaving a white tip (Marsden, 1962). The snail also digested tissue and left the skeleton unmarked but from the base of the coral and in an unsystematic manner; filamentous algae covered the bared area quickly. Table 4 displays the frequency of predation by these four animals in the three study areas. Diadema attack was more common on the west fore reef whereas damsel fish damage was prevalent on the east side. Considerably more corals in the back reef show predation-almost entirely from damselfish (Williams 1978 TUNNICLIFFE: CARIIlI3EAN STAGHORN CORALS 143 describes a vigorous damselfish population in this area). Overall more than a fifth of the corals had obviously been attacked by predators. An estimate was made of the extent of damage inflicted by damselfish. These fish are territorial and construct "gardens" in the staghorn corals by quickly killing an area of live branches and defending the subsequent algal growths. Twenty stations were examined using 4-m2 quadrats at each; active damselfish gardens occupied 6% of the total area. The mean size of a territory defended by a single 2 2 fish was 2,430 cm (s = 1,400; n = 26) or about 1f4 m • Of the 26 gardens present in October 1977 and followed to March 1979, one-half did not span that entire time: the fish migrated elsewhere (or died) sometimes leaving prolific algal gardens. On the other hand, some gardens were stable for the period and the fish were inflicting no further damage on the coral population. The back reef transect sup- ported more damselfish and their gardens occupied about 15% of the area. Before 1980 the disease dubbed "white death" (described by Antonius, 1977) in which a coral appears to "shut down" and lose its tissue within one day, was seen only occasionally at Discovery Bay. During the summer of 1980 the spread of white death in the A. cervicornis population became marked. Its effect was chronic after Hurricane Allen taking a large toll of the surviving fragments (Knowl- ton et aI., 1981). Sediment was a small hazard on the haystacks of the fore reef where little was deposited but mortality due to smothering in the back reef was evident. Most of the deeper corals were lodged in the sand and their lower portions were dead (Fig. 4c). Overgrowth of A. cervicornis by other organisms was not important; this coral avoids most neighbors by its rapid growth rate and height above the substratum. The boring sponge Cliona aprica was the most frequent neighbor. The holes it creates are instrumental in the weakening of the coral structure (Tunnicliffe, 1979) but it does not actively kill coral tissue.

Post Mortality Processes High population numbers, rapid growth rate and high mortality resulted in the accumulation of large amounts of skeletal debris from A. cervicornis. This rubble has three possible fates: (1) it may stay in place, compacting to form the "rigid framework" (Goreau and Goreau, 1973) of the reef; (2) it may be transported and deposited as talus at the base of the deep fore reef slope (Goreau and Land, 1974); or (3) it may be converted to smaller fragments by dissolution and erosion to form the "clastic framework" (Goreau and Goreau, 1973) in which the finer detritus is deposited in the gaps of the rigid framework. The distributions of both dead and live coral on the Pinnacle Two transects are graphed in Figure 9. The overall amount of dead branches on the reef surface- as seen from the photographs- was similar to that of the live A. cervicornis. The peaks of dead coral were slightly offset from those of the live, suggesting that there was some transport down the reef. The final peak in the dead coral was over the haystack edge where debris easily accumulates. A Spearman correlation between the amounts of dead and live coral at each sample station (n = 20) was insignif- icant. However, if the values for the dead coral are shifted back by 10m (horizontal distance), the test becomes significant at P = .02. When a 20-m shift is performed, the correlation again becomes insignificant. The open network of dead branches forms hiding places for numerous mobile animals. Algae and the foram Gypsina bind the dead branches together although it was not difficult to disassemble them by hand. Below the top 20 cm the peys- 144 BULLETIN OF MARINE SCIENCE. VOL. 33. NO. I. 1983

Table 5. Calcium carbonate production by corals on the reefs of Discovery Bay. Abundances of the four major corals were measured on Pinnacle Two reef and in Damsel Gardens; 'other corals' are estimates

Skeletal Fore Reef Back Reef Density Growth Rate Production Production Coral (g/ee) Source cm/yr Source kg/ml/yr kglm'/yr Acropora cervicornis 2.3 2nd yr growth 12.0 88 branches 1.4 0.1 Man/as/rea annularis 1.8 Dustan (1975) 0.6 Dustan (1975) 1.1 1.0 Colpophyllia na/ans .65 s =.10 1.5 estimate 0.3 .04 n = 26 Porites as/reoides J.3 s = 0.1 0.96 Vaughan (1915) 0.1 0.3 n=8 Other corals 0.3 0.3 Total Production CaCO, (kglm2/yr) 3.2 1.7

sonneliaceaen algae were most abundant. An open A. cervicornis framework was evident in a hole dynamited 5 m into a haystack at Montego Bay; this far below the reef surface small sclerosponges continued the internal process of binding (Hartman and Goreau, 1970). The rapid growth rates of this coral combined with the high skeletal density and the evidence of high rates of mortality suggest that there must have been a large accumulation of skeletal material from A. cervicornis on the reef. Assuming the average density of a coral branch to be 2.3 glcm3 and diameter to be 1.5 cm, the standing crop of 1,000 cm/m2 of staghorn branches would be 4.06 kglm2• If annual production was 35 branches per square meter, the contribution of new growth was only about 0.34 kglm2-small due to low density of the branch tips. The subsequent year's infilling increased the density from about 1.2 to 2.2 glcm2 therefore adding about 1.05 kglm2/yr. Annual production of calcium carbonate by A. cervicornis was around 1.4 kglm2 a value which compares well with that of 1.2 kglm2 estimated by Land (1979). This value is about a third of the standing crop value which suggests a high death rate; Land (1979) estimated a turnover time of 4 years for a colony. Similar productivity estimates were made for the other major corals of the Discovery Bay reefs. These figures are presented in Table 5 for both the fore and back reef areas. The value for contribution by unmeasured corals is a guess; the most significant of these were probably Agaricia spp., Porites porites, Dip/oria spp., and Siderastrea spp. The value for back reef production is for a small area only; most of the bay has no corals. The final total of coral production in the 2 l cervicornis zone between 5 and 20 m is 3.2 kg·m- ·yr- • Land (1979) estimated the contribution by M. annularis to be twice that I calculated; his final productivity 2 l value for this zone is 5.2 kg·m- ·yr- • Smith and Kinsey (1976) used CaC03 mass balances in the water to calculate coral production at 4 kg·m-2·yr-I on Pacific reefs. A. cervicornis and M. annularis are the major producers but A. cervicornis material is more quickly available for reef construction and as a substratum.

Other Scleractinians Three other scleractinians were examined for their distributions. These data were not originally gathered for the purposes of comparison and methods are not consistent. The distributions of these corals and that of A. cervicornis are presented TUNNICLIFFE: CARIBBEAN STAG HORN CORALS 145 in Figure 10. M. annu/aris was a dominant coral in the mixed zone. Dustan (1975) presented a comprehensive survey of this coral on a nearby haystack of Discovery Bay. The peak 250 m from the crest is an artifact as the transect pivoted delib- erately on a large, outstanding head of M. annu/aris. The upper reef, in the mixed zone, has the most extensive coverage by the massive corals. In general, their abundance increased where that of A. cervicornis fell. These corals probably com- peted for space. To test the hypothesis of mutual exclusion, a non-parametric correlation tested the significance ofthe negative relationship between the values for A. cervicornis and M. annu/aris coverage (because the other two corals were measured for continuous coverage, a useful test was not possible). For a sample size of 17 quadrats, the negative Spearman correlation coefficient was significant at P < .02. On the back reef transect, this inverse relationship between A. cer- vicornis and the massive corals was not significant. Population densities may have been too low for a competitive interaction to manifest itself. In the shallow areas of the east fore reef small heads of P. astreoides were common. C. natans had a constant but low coverage as small colonies from 6 to 26 m. M. annu/aris was common but did not form the large heads of the mixed zone on the west fore reef. Other massive species were abundant-particularly those of Dip/oria and Siderastrea. Abrasion and mechanical damage of these corals from fallen branches of A. cervicornis were frequent. C. natans was greatly affected as it has a very low skeletal density (x = 0.56 glcm3; s = 0.05; n = 9) and is susceptible to erosion. Large colonies ofbrain corals were often completely bissected by a fallen stick of staghorn coral (Fig. 4d). Despite the open lattice-work of A. cervicornis branches, the corals appeared to reflect much light. Attenuation studies were conducted under A. cervicornis: "The A. cervicornis appeared to act as a neutral density screen reducing the irradiance levels (PAR 300-700) to 22 to 44% of the irradiance level directly above the branches" (Dustan et al., in prep.). There were numerous small corals on the A. cervicornis rubble below the live branches but large ones were rare. The most abundant coral in this unfavorable habitat was the foliose Helioseris cu- cuI/ala.

DISCUSSION The reefs of Discovery Bay, Jamaica supported at least three A. cervicornis assemblages that were distinct both in their coral composition and the physical environment. The major expanse of fore reef west of the ship channel was com- prised of large haystacks that supported dense populations of A. cervicornis. The upper limit of the A. cervicornis population appeared to be defined by wave forces; deeper, the waves of Discovery Bay rarely harmed the fragile A. cervicornis but a shallower habitat or high waves exceeded the coral's strength (Tunnicliffe, 1982). The lower limits of the population were probably set by low light levels or the presence of steep cliffs on which purchase for the staghorn fragments was difficult. The second assemblage was that of the east fore reef where the extensive plat- form had little topographic relief; A. cervicornis was sparse. The third community in the back reef was influenced by the mobile sediments. Mound corals, boring sponges, and in the deeper "sand" assemblage, A. cervicornis predominated. That the west fore reef corals were generally larger indicates that they may have experienced more satisfactory growing conditions or were more vigorous. The stunted conditions of the back reef corals may be due to suspended sediments (Dodge et al., 1974) although the east fore reef corals showed similar size char- 146 BULLETIN OF MARINE SCIENCE. VOL. J3. NO. I. 1983 acteristics. Perhaps the fore and back reef corals of the east side were of the same genetic stock. The reef crest does not come to the surface so the two populations might have communicated by larvae or seedling fragments. Transplantation ex- periments would be useful. Inter-habitat variations in coral morphology have been previously noted (Go- reau, 1963; Roos, 1971; Brakel, 1976). As does Acropora palmata (Graus et a!., 1977), A. cervicornis morphology may have responded to wave intensity: higher branching orders were found in the shallower water. The shallow corals had higher growth rates but these were not reflected in the corals' heights; instead, the corals were branching more frequently perhaps to avoid exceeding an upper size limit above which the waves would cause extensive breakage. Over the course of 5 years many corals were examined but from these only two larvae were captured from the animals held in the laboratory. A. cervicornis recruits almost entirely by vegetative spreading. Instability of staghom corals increases with greater height (therefore bending moment) and erosion by boring sponges; the coral then breaks. Small fragments usually die but the larger pieces re-establish and grow (Tunnicliffe, 1981). Contact between such "sister" fragments may have resulted in the frequent grafts that showed complete tissue acceptance. Varying grades of fusions between colonies appeared to represent stages in the acceptance of contacting tissues. The recognition of self has been described for other invertebrates (Theodor, 1970; Hildemann, 1974). Hildemann et al. (1975) described an immuno-incompatibility response between colonies of Acropora formosa. but there the allograft suture zone was devoid of tissue. It may be that because of the vegetative expansion of the A. cervicornis population only a limited number of genotypes were present that could be detected by graft responses. The continual breakage and regrowth of fragments was probably responsible for the lack of pronounced orientation in the growth of the staghom branches. Branches may have responded to flow direction through an actual sensing capacity as suggested by Graus et a!. (1977) but such trends did not become established. The majority of corals on this reef have been broken at some time (Tunnicliffe, 1979) and this proportion approached 100% after Hurricane Allen (unpubl. data). Corals of the genus Acropora generally have high growth rates. A. pulchra. a Pacific species, can grow 17 cm/yr (Tamura and Hada, 1932). Vaughan (1915) reported low rates of 4.0 cm/yr for Aoridian A. cervicornis although Shinn (1966) subsequently measured increments of 10 cm/yr. Lewis et a!. (1969) measured monthly increments of staghom in Barbados and Jamaica: from the former rates of 12 cm/yr and for the latter 14.4 cm/yr can be calculated from their data. Rates from this study agree well and indicate that light is a major controlling factor of rates. Skeletal density is unaffected by environmental variations and appears to be species specific. A. cervicornis is the densest coral I have measured and is approached by only Dichocoenia stellatus (2.3 glcm3; s = 0.07; n = 15) and per- haps Dendrogyra cylindricus. There is a misleading tendency in much of the pertinent literature to assume that A. cervicornis is very porous because of its high extension rates. Predation, shading, mechanical abrasion and overgrowth were the major causes of death outside occasional outbreaks of disease and major storms (Woodley et a!., 1981). Frequent breakage and fragmentation of this coral resulted in injury and mortality, the extent of which depended on the amount of tumbling and the type of substratum under the fallen pieces. The large amount of breakage in the A. cervicornis of the sandy deep back reef was initially perplexing. In the first place, the presence of such a large coral population there was odd as the shifting sand substratum would discourage settlers. It is likely, therefore, that the entire Tl 'NNICLI FFE: ('ARIlIBEAN STA

"sand" staghorn population had shifted. Waves moving over the reef crest en- couraged down-slope transport in this area of the back reef thus the farther they moved the more fracture they incurred-hence, the correlation observed between breakage and depth here. The urchin Diadema antillarun grazes non-coral surfaces in its quest for algae. Rarely is it reported as a predator of live coral although Bak and van Eys (1975) comment on the attack on A, cervicornis, among other corals. Five percent of the staghorn coral in my study had been recently attacked in their basal portions by the urchin. Diadema was rarely seen among the upper branches of A. cervicornis; perhaps the small purchase area and coral nematocysts deter the urchin from such climbing. No doubt Diadema significantly increased the bioerosion rate of the reef by its feeding habits as was noted in Barbados (Stearn and Scoffin, 1977). Ott and Lewis (1972) recorded feeding rates of coral predators in Barbados and concluded that neither the snail Coralliophifa nor the polychaete Hermodice caused extensive mortality: they did appear to be the least significant here. In contrast, 13% of all A. cervicornis examined had been damaged by the three-spot damselfish. However, my measurements do not agree with those of Kaufman (1977) also working in Jamaica, who suggests that 10 to 40% of the fore reef terrace is under active algal lawn; in my west fore reef site the value was 6%. The high growth rates and ensuing high mortality of A. cervicornis resulted in a large contribution to skeletal calcium carbonate on the reef which must have a marked effect on the vertical accumulation of the reef. The most extensive pop- ulations are atop the haystacks. Caribbean reef accumulation appears to have matched the rise of the early Holocene sea level at about 8 01/ 1,000 years (Adey, 1975; Adey and Burke, 1976; Shinn et aI., 1977). The Mexican Holocene section analyzed by Macintyre et al. (1977) showed an initial accretion of about 6 m/ 1,000 years in a community dominated by massive corals but a later shift to an A. cervicornis community doubled the accumulation to 12 m/l ,000 years. As the reef builds toward the surface wave influences become stronger; in many parts of the Jamaican reefs this process results in a reduction of the shallow A. cervicornis community and formation of a vertical seaward wall (Goreau and Goreau, 1973). The reefs of the eastern Caribbean are exposed to high wave activity and the growth of A. cervicornis is limited. Macintyre et al. (1977) speculated that reef accumulation around the western protected islands is much higher because of the preponderance of this coral. Wave energy dictates the presence of A. cervicornis which then affects rate of reef accumulation (Adey, 1978). The fragility of stag horn appears to limit its growth to depths greater than 5 m in areas where waves are often 2 01 in height (Tunnicliffe, 1982). For a structure as inherently unstable as A. cervicornis the presence of large drag forces combined with the weakening effects of boring sponges results in frequent breakage. However, it appears that the coral's growth effort is invested in continual budding and somatic replication rather than sexual reproduction. Regrowth from fragments is common and the coral population thrives at moderate levels of wave activity and breakage. Invasion of shallower habitats by acroporids did not occur in the Caribbean region until the early Pleistocene when the large structurally sound form of A. pafmata invaded the reef crest zone (Tunnicliffe, 1980a). Figure 11 is a schematic of the interactions in a staghorn community stressing the cyclical nature of the processes which maintained and augmented the coral population. If success is measured by numbers then the larger part of the west fore reef between 5 m and 30 m represented a highly successful habitat for A. CCf'I'icornis.The competitive dominance of this coral was maintained by two major features of the coral's growth patterns: its rapid growth rate and its ability to 148 BULLETIN OF MARINE SCIENCE. VOL. 33. NO. I. 1983

obraslon

( ptl!datlon /SELF.SHADING ~

GROWTH DEAD BASE

~ SPONGE/

REATTACHMENT REGROWS ~ ~ CLiONA SETTLES

DIIIPt:RSAL OF / CORAL AND SPONGE

STRUCTURE WEAKENS

IfOQrntfttatton) ~

...------wov~ s.ur;l!! BREAKAGE '.II',.::-V flelQhbOu/ '

FRACTURES COIoIPOUND

~ GltAFTlNG /III IlEATH III BREAKDOWN COIIIIUN IT Y BIlOWTH

_' ••n~"" ~

REEF aliLD-uP

Figure 11. Schematic of the cycle of an Acropora cervicornis population. establish new structures after breaking. The effects on organisms competing for space were three-fold: (I) the "upper-storey" growth of staghorn branches soon shaded encrusting corals and algae thus reducing their growth (a similar phenom- enon is described by Connell [1976] on Australian reefs); (2) falling staghorn corals may cause severe damage to underlying corals which cannot rapidly recover (Fig. 4d); and (3) while sexual recruitment by other coral species may be a seasonal phenomenon (Stimson, 1978) the staghorn population continually claimed new space with the aid of eroding sponges and high wave activity throughout the year. Connell (1978) draws numerous parallels between ecological processes on reefs and in tropical forests. Many aspects of the growth of both the staghom population and the single coral are reminiscent of plants. Its vegetative reproductive mech- anism results in a consolidation of the local population and rapid increase in numbers-a phenomenon also seen in plants such as the trembling aspen (Grime, 1979) and certain species of marginal habitats (Billings and Mooney, 1968). A. cervicornis appears to display attributes of both the r- and the K-strategist. It fits well into Grime's (1977) C-strategy category for plants selected for high compet- itive ability in productive environments; they often have rapid vegetative expan- sion and asexual reproduction. These aspects of the growth of A. cervicornis render it susceptible, however, to extreme conditions. Violent storms will destroy staghom thickets beyond recovery (Stoddart, 1974); the devastation by Hurricane Allen in Jamaica (Woodley et al., 1981) has left doubt that the A. cervicornis community described here will recover TUNNICUFFE: CARI13BEAN STAGHORN CORALS 149

(Knowlton et aI., 1981). Its low propensity for sexual reproduction may limit its ability to recolonize the reef.

ACKNOWLEDGMENTS

Numerous suggestions for the direction of this research came from Dr. W. D. Hartman, Prof. G. E. Hutchinson, and Dr. D. C. Rhoads. I am indebted to S. Ohlhorst, J. Lambiase, and J. Oland as well as the Discovery Bay Marine Laboratory for both corporeal and mental assistance in the field. Welcome suggestions came from Drs. B. Tiffney, M. de Burgh and two reviewers. The research was funded by National Science Foundation (OCE 78-06731 to the author), the Canadian Federation of University Women, and the Woman's Seaman's Friend Society of Connecticut. In partial fulfillment of requirements for doctoral degree from Yale University. This is Contribution Number 266 from Discovery Bay Marine Laboratory.

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DATE ACCEPTED: June 8, 1982.

AIlDRISS: Department of Biology. Yale University. New Haven. Connecticut. PRESENT ADDRESS: Bi- ology Department, University of Victoria, Victoria. B.C. V8 W 2Y2, Canada.