Diadema antillarum - IngentaConnect

BULLETIN OF MARINE SCIENCE, 68(2): 327–336, 2001

CORAL REEF PAPER

RECENT POPULATION DYNAMICS OF DIADEMA ANTILLARUM AND TRIPNEUSTES VENTRICOSUS ALONG THE NORTH COAST OF JAMAICA, W. I. Christopher S. Moses and Rena M. Bonem ABSTRACT Prior to 1983, the black spiny sea urchin, Diadema antillarum, was ubiquitous on Caribbean reefs. Jamaica was no exception to this, as D. antillarum represented the primary herbivore on the overfished reefs of the island. Then, in 1983, D. antillarum populations were struck by a mass mortality throughout the Caribbean reducing the number of these urchins in places by 85–100%. Since that time, Jamaican D. antillarum populations have been slow to recover. In 1998, populations along the north coast of the island had only recovered to, at most, 5–10% of their original densities. Normally restricted to back reef and lagoonal grass beds, another species of echinoid, Tripneustes ventricosus, began to show increased numbers on the forereef in 1996–1998 in the vicinity of Discovery Bay, Jamaica. These sea urchins now seem to be competing for the niche once dominated by D. antillarum and helping to increase the grazing pressure on these algal dominated reefs.

Sea urchins are the most ravenous invertebrate herbivores. In a place like Jamaica where the populations of herbivorous fishes have been greatly reduced (Jackson, 1997), sea urchins (Echinodermata: Echinoidea) are the chief grazers on the reef. Prior to 1983 the black spiny sea urchin, Diadema antillarum, was omnipresent on the north coast of Jamaica (Carpenter, 1981; Sammarco, 1980; Sammarco, 1982; Hughes et al., 1985, 1987; Jackson, 1997). In some back reef locations in Discovery Bay, populations of these sea urchins as high as 71 urchins m−2 were recorded in 1973 (Sammarco, 1980). On the forereef at Discovery Bay, the density of D. antillarum was not quite as high as in the back reef, averaging about 10–12 urchins m−2 in the shallow mixed zone and about 4 urchins m−2 at depths of −15 m on the forereef terrace (Hughes et al., 1985, 1987; Liddell and Ohlhorst, 1987). Even at depths as great as −30 m on the forereef slope, D. antillarum could be found in populations averaging 0.1 urchins m−2 (Liddell and Ohlhorst, 1987). Hurricane Allen (1980), greatly reduced populations of D. antillarum in Jamaica to as low as about 6 urchins m−2 in many shallow areas (Woodley et al., 1981), but only 16 mo later, the populations rebounded, surpassing pre-hurricane numbers which were as high as 13 urchins m−2 (Woodley et al., 1981; Aronson, 1993). Despite, the apparent good health of this large echinoid population, disaster befell the D. antillarum community beginning in January 1983 in Panama and spread throughout the Caribbean. The north coast of Jamaica was no exception and provided no safety from the supposedly water-borne, species-specific pathogen which began to affect urchins there in July 1983 (Lessios et al., 1983, 1984; Hughes et al., 1985, 1987; Liddell and Ohlhorst, 1987; Hughes, 1994). Since the near extinction of the species in Jamaica, D. antillarum populations have not recovered. Studies by Lessios (1988, 1995) also show this lack of recovery in Panama where the mass mortality began. The loss of these urchins leaves a window of opportunity for another herbivore to establish its dominance on the reefs. However, not until the recent expansion of Tripneustes ventricosus populations onto the forereef has there been 327

328

BULLETIN OF MARINE SCIENCE, VOL. 68, NO. 2, 2001

any apparent shift to fill the niche left vacant by D. antillarum for more than 15 yrs in Jamaica (Bonem and Moses, 1998). MATERIAL AND METHODS We chose four reefs along a 10 km stretch of the north coast of Jamaica, centered at Discovery Bay, for this project (Fig. 1). The following locations are for moorings or anchoring locations used at each site: LTS (18°28.40'N, 77°24.82'W); Pear Tree Bottom reef [PTB] (18°27.80'N, 77°21.44'W); East Rio Bueno reef [ERB] (18°28.84'N, 77°26.99'W); Dairy Bull (18°28.07'N, 77°23.63'W). In May and June 1998 as part of another project, LTS, Pear Tree Bottom reef, and East Rio Bueno reef were mapped for bathymetry and morphology (Moses, unpubl. data). Dairy Bull had been mapped previously by both Cochran (1996) and Gaitros (1996). For sea urchin population density surveys, the technique used is a modification of the common meter square grid methods. A 1 in (2.54 cm) outer diameter PVC pipe was placed vertically into a crack in the reef at the desired depth. Then, from that point, 10 m transect lines were laid perpendicular to each other, outlining a box that covered 100 m2. The divers then swam systematically within that area, checking all crevices, and counted all the urchins they could find. Because patchiness of urchin distribution is less than the area surveyed, this technique minimized the problems associated with having clumps of urchins or areas with none at all and helped find a better average population. This method of population measurement was applied at each of the four sites at depths below surface of 1.5, 3, 5, 6, 7, 9, 11 and 12 m. Within this depth range, the morphology of these reefs is a sufficiently low angle that the large grid did not cover a depth range that extended into the next sampling depth. Because of the extent of the grid, it was positioned such that the average depth (with minimal variance) was the desired depth. Each reef was surveyed a total of five times for urchin density over the above mentioned depth range. The multiple surveys of each reef were performed on different days, but in each case, the total of five surveys was completed in a period 7 d or less.

Figure 1. Location map of the study sites and their relative positions along the north coast of Jamaica.

MOSES AND BONEM: DIADEMA AND TRIPNEUSTES IN JAMAICA

329

Table 1. Previous population densities of Diadema antillarum in the area of this study (urchins m−2). *The column of data from 1986 is entirely from Hughes et al. (1987) and is a resurvey of all of the sites listed here. Dancing Lady, Mooring 1, Water Tower, and Zingorro are all buttresses of the Discovery Bay forereef very similar to LTS. Dancing Lady is about 20 m east of LTS, and Mooring 1 is about 200 m east of LTS. Water Tower reef and Zingorro reef are both about 500 m west of the Discovery Bay ship channel. Modified from Hughes et al. (1987). Location Crosby Patch Reef (lagoonal) Dancing Lady Mooring 1 Water Tower/Zingorro

Pear Tree Bottom Rio Bueno

Depth (m) 2 8 15 3 10.5 5 15 22 10 7 10 20

Before die-off Source 71.0 Sammarco, 1982 10.5 Hughes et al., 1985 4.7 8.1 Carpenter, 1981 12.2 6.1 3.2 Liddell and Ohlhorst, 1987 2.2 8.9 11.7 3.5 0.7

Hughes et al., 1985 Hughes et al., 1985

1986* 0.80 N/A N/A N/A 0.15 0.45 -

RESULTS AND DISCUSSION DIADEMA ANTILLARUM POPULATIONS.—Despite the fact that Hughes et al. (1985) predicted that the high fecundity and density of planktonic larvae of D. antillarum would cause its diminished counts to be short-term, time has shown otherwise. In fact, it is likely that because of the external fertilization mode, a certain population density must be achieved before a substantial growth in the population can be expected from reproductive events (Lessios, 1988; Hughes, 1994). If there are only a few urchins in the area, the chances of their gametes meeting and successfully fertilizing in the water column is orders of magnitude lower than with higher population densities. According to Hughes et al. (1987), by 1986 populations had recovered to a maximum of only 10% of their pre-1983 numbers. In many locations, by 1986, the populations had only recovered to 2–3% of their original counts (Table 1). Until recently, the recovering populations of this species were limited to water shallower than 6 m, and individuals were only rarely found below this depth. The distribution of Diadema with depth was shown to be significant (two-way ANOVA; P < 0.005) as was the variation in population densities from one site to another (P < 0.03). This confinement to shallower water was probably a result of reduced populations and increased food availability at those depths. At the time this study was performed in 1998, the populations have not yet seen any substantial growth since 1983. Besides their slowly increasing population density, we also noted changes in the distribution of D. antillarum populations. These urchins are beginning to expand their habitat into deeper locations. In fact, some are found at depths as great as 9 m, albeit in small numbers (Table 2). This is the first time since 1983 that D. antillarum have been seen regularly at such depths. This expansion down the reef could be a result of a number of factors, but can be taken as an indicator of increasing, rather than merely migrating, sea urchin populations.

330


Table 2. Population densities of Diadem antillarum and Tripneuste ventricosus in June 1998. Depth (m)

D. antillarum/m2

T. ventricosus/m2

LTS

1.5 3 5 6 7 9 11 12

0.22 (±0.07) 0.65 (±0.43) 1.15 (±0.28) 0.24 (±0.23) 0.03 (±0.02) 0.01 (±0.01) − −

0.11 (±0.04) 0.13 (±0.10) 0.24 (±0.05) 0.79 (±0.13) 0.61 (±0.12) − − −

Pear Tree Bottom

1.5 3 5 6 7 9 11 12

0.16 (±0.04) 0.43 (±0.15) 0.92 (±0.11) 0.11 (±0.05) 0.03 (±0.01) 0.02 (±0.02) − −

0.14 (±0.06) 1.61 (±0.33) 2.14 (±0.10) 0.17 (±0.05) 0.02 (±0.01) − − −

East Rio Bueno

1.5 3 5 6 7 9 11 12

0.07 0.08 0.27 0.01

0.05 (±0.02) 0.33 (±0.11) 0.53 (±0.22) 0.02 (±0.01) 0.01 (±0.00) − − −

Dairy Bull

1.5 3 5 6 7 9 11 12

0.25 (±0.05) 1.85 (±0.29) 1.56 (±0.20) 0.74 (±0.11) 0.07 (±0.04) 0.03 (±0.01) − −

Location

(±0.06) (±0.07) (±0.16) (±0.02) − − − −

0.28 0.11 0.04 0.03 0.06 0.08

(±0.07) (±0.11) (±0.04) (±0.01) (±0.03) (±0.03) − −

In 1982, populations on the forereef were as high as 10.5 urchins m−2 at 8 m, and 4.7 urchins m−2 at 15 m. One month after the disease struck in 1983, these populations had been reduced to 0.2 urchins m−2 at 8 m, and 0.1 urchins m−2 at 15 m (Hughes et al., 1985). When the urchin surveys for this project were conducted in June 1998, the highest density of D. antillarum at LTS was at 5 m with a population density of 1.15 urchins m−2. From there, the numbers decrease with depth until there are only 0.01 urchins m−2 at 9 m, and none found below that. At 7 m, there are only 0.03 urchins m−2, 0.28% of the density reported for 1982 at 8 m by Hughes et al. (1985). Despite the reduced populations of D.


331

Figure 2. Photograph of Diadema antillarum (Da) and Tripneustes ventricosus (Tv) at 5 m at Pear Tree Bottom reef. This photograph illustrates the fact that the two urchin species are now occupying the same section of the forereef. Notice the bare substrate exposed by the grazing of the urchins in this area. Areas of this reef without colonies of urchins can have more than 75% cover by macroalgae (Moses, unpubl. data). The Diadema antillarum can also be seen in this photograph to prefer cracks and crevices to the more overt positions chosen preferentially by Tripneustes ventricosus (daylight observation only in this study).

antillarum at this site, Perry (1999) reports that these urchins still exert a significant force of bioerosion on the shallow forereef (at 5 m) from their grazing. In 1982, a population density of 8.9 urchins m−2 was reported at 10 m at Pear Tree Bottom reef (Hughes et al., 1985). This survey found only 0.02 urchins m−2 at the same depth in June 1998—greater than 99% less than the original population on this reef. The highest concentrations of D. antillarum at Pear Tree Bottom reef are at 5 m, the same as LTS, with a density of 0.92 urchins m−2. In 1983, after the blight, there were no urchins present at Pear Tree Bottom below 6 m, but today they extend as deep as 9 m (Fig. 2). Hughes et al. (1985) reported that Rio Bueno had only about 60% as many urchins as LTS did at many depths. The reason for this low number is not known, but the trend is continued in current data as the East Rio Bueno site has the lowest urchin counts. In fact, the peak density, as with the other two sites, lies at 5 m and is only 0.27 urchins m−2. Bak (1985) showed that any kind of fouling of substrate, including algae, reduced recruitment of Diadema. At this site, very high algal densities lead to the availability of 80% macroalgal cover at many depths (Moses, unpub. data). Dairy Bull reef was recently surveyed for urchins in a pair of studies in 1996 (Cochran, 1996; Gaitros, 1996). However, the numbers for urchin population densities presented in

332


Figure 3. (a) Graph of the population distribution of Diadema antillarum at each of the four sites. Analysis by two-way ANOVA showed that the distribution of population by depth at all sites was significant (P < 0.005) and that variance from reef to reef was also significant (P < 0.03); (b) Graph of the population distribution of Tripneustes ventricosus at each of the four sites. Analysis by twoway ANOVA of Tripneustes populations revealed that their distribution was not significantly related to depth overall (P = 0.21) [except at PTB where the relationship was significant (P < 0.004)] and that the variation in their population from reef to reef was also insignificant (P = 0.22).

those studies seem unusually large in comparison with the preliminary observations at Dairy Bull for this study as well as the observations at the other sites. For their methods, Cochran (1996) and Gaitros (1996) both used meter square grids laid along a transect line to count urchin density. This method, or perhaps a bias in the way the transects were laid, could potentially be the source of error in this case. D. antillarum have a tendency to form clumps or small congregations in which the density in one square meter can easily reach 10 urchins m−2 even today. However, outside these clumps, population densities often approach zero for several meters in any given direction. Thus, a transect line laid through a series of these clusters is not an accurate representation of the true population density. Using the method from this paper, the population of urchins at Dairy Bull was reexamined. Previous estimates by Cochran (1996) and Gaitros (1996) report D. antillarum densities ranging from 10 urchins m−2 in shallow water to 1 urchin m−2 at greater depths. After resurveying, Dairy Bull does, indeed, have the highest concentrations of this species of any of the sites in this study. However, the population density peaks at only 1.85 urchins m−2 at a depth of 3 m (Fig. 3A). In respect to data from post-mortality studies of this species in this region (Hughes et al., 1985; Hughes et al., 1987; Liddell and Ohlhorst, 1987; Hughes, 1994), this number seems much more accurate and is, in fact, probably about 10–15% of the original density at this site. TRIPNEUSTES VENTRICOSUS POPULATIONS.—T. ventricosus, also known as the ‘sea egg’, is a white-spined sea urchin with an adult test diameter averaging 7–10 cm, with much shorter


333

spines than D. antillarum. Populations of these urchins are well established in the back reef and lagoonal areas of Jamaica and their conspicuous presence there pre-dates the mass mortality of D. antillarum (Keller, 1983; Woodley et al., 1999). In the lagoons, T. ventricosus distinguishes its territory from that of D. antillarum by preferring open Thalassia grass-beds to the patch reefs preferred by the D. antillarum (Ogden et al., 1973; Keller, 1983; Hughes et al., 1987; Woodley et al., 1999). Before the mass mortality of D. antillarum in 1983, T. ventricosus was restricted to the lagoons, and seldom seen on the forereef (Woodley et al., 1999). Woodley (1999) and Woodley et al. (1999) began to notice significant increases of T. ventricosus at the CARICOMP site on the forereef of Discovery Bay as early as 1996. While we noticed the localized populations of T. ventricosus on the forereef at Discovery Bay, it was not until May, 1998 that a dive at Pear Tree Bottom reef (about 5 km to the east of the CARICOMP site) showed that there had been a more widespread change in the population and distribution of T. ventricosus. A preliminary qualitative survey conducted at the beginning of this study estimated that the numbers of these urchins on the forereef was beginning to rival the populations of D. antillarum. In fact, the later quantitative surveys showed this initial observation to be correct (Bonem and Moses, 1998). We also noticed that T. ventricosus appeared to prefer non-cryptic, higher positions on any given area of the reef, in contrast to the more cryptic nature of D. antillarum (Fig. 2). With urchin populations near zero at LTS in recent years, the changes there are a dramatic shift. T. ventricosus is found between 0 m and 7 m at LTS. Peak concentrations of these urchins occur at 6 m, a depth where D. antillarum at this reef showed a rapid decline in population, relative to shallower densities here. At 6 m, T. ventricosus populations reached as high as 0.79 urchins m−2, possibly due to the lack of D. antillarum at this depth (Fig. 3B). Pear Tree Bottom reef has the highest concentrations of T. ventricosus of any of the four sites measured. At this reef, the peak densities of both species of urchins occur at the same depth (5 m). At this depth, T. ventricosus densities are 2.1 times higher than their lagoonal average of about 1 urchin m−2 (Keller, 1983), and 2.3 times higher than those of D. antillarum at the same location. However, the population falls off sharply after 5 m to a density of only 0.02 urchins m−2 at a maximum depth of 7 m. This reef is the only site in this study that shows a significance to the distribution of Tripneustes on the forereef with depth (one-way ANOVA; P < 0.004). At East Rio Bueno reef, T. ventricosus populations outnumber D. antillarum populations across about 90% of the reef. Similarly to Pear Tree Bottom, both populations of sea urchins prefer the same depth on the reef. For both species, the highest densities fall at 5 m, at 0.53 urchins m−2 [T. ventricosus] (Figs. 3B,4). Because of its morphology, this reef exaggerates the spatial separation between the two species of urchins in relationship to T. ventricosus preferring less cryptic locations than D. antillarum. As an example of how limited the populations of T. ventricosus have been on the forereef in the past, Cochran (1996) and Gaitros (1996) did not consider this urchin numerous enough at Dairy Bull reef to have any impact on reef condition. Dairy Bull does, in fact, have the lowest overall densities of T. ventricosus of the study sites, reaching a maximum of only 0.28 urchins m−2 at 1.5 m on an algal-covered cliff as it extends below the surface. With the high populations of D. antillarum that exist at Dairy Bull, it is logical that this higher competition for resources, as well as the lack of a back reef lagoon, limited the number and scope of the T. ventricosus population at this site.

334


Figure 4. Graph of the average population distributions of both species of urchins throughout the study area (variance listed in table 2). In depths shallower than 6 m, Diadema antillarum maintains noticeably higher population densities than Tripneustes ventricosus. Also note that the peak populations of both urchins occur at 5 m. High density at this depth is probably due to a favorable combination of lower wave energy, yet sufficient algal abundance.

CONCLUSIONS This study illustrates a shift in niche occupation on the forereef along the north coast of Jamaica. Where D. antillarum was once ubiquitous and clearly dominant, then suddenly nearly extinct, T. ventricosus is now moving in and taking advantage of the abundant food source. At the same time, D. antillarum populations along the north coast are showing signs of continuing a slow recovery. Combined, the total numbers of urchins (thus herbivores) is increasing more rapidly now than at any time during the previous 15 yrs. The moderately increasing populations of D. antillarum and the immigration of T. ventricosus to the forereef in Jamaica could begin to cause the reduction of macroalgae on the forereef, generating more bare substrate, aiding in coral recruitment and recovery of this reef ecosystem to its previously coral-dominated state. ACKNOWLEDGMENTS This research was supported in part by a grant from the Baylor University Department of Geology. Thanks goes out to S. Dworkin and D. Vodopich of Baylor University, and M. Vierros of UNEP who gave their constructive criticism of this project. Also, a special thanks to the staff of the Discovery Bay Marine Lab, U.W.I. who kept the boats running and the scuba tanks full. Thanks to C. Carrell, a tireless and capable dive buddy. This is contribution #619 from the Discovery Bay Marine Lab, U.W.I.


335

LITERATURE CITED Aronson, R. B. 1993. Hurricane effects on backreef echinoderms of the Caribbean. Coral Reefs. 12: 139–142. Bak, R. P. M. 1985. Recruitment patterns and mass mortalities in the sea urchin Diadema antillarum. Proc. 5th Int’l. Coral Reef Congr., Tahiti. 5: 267–272. Bonem, R. M. and C. S. Moses. 1998. Niche expansion, competition and reef dominance, Implications for the geologic record. In Abstracts with programs, GSA annual meeting. 30(7): A-29. Carpenter, R. C. 1981. Grazing by Diadema antillarum and its effect on the benthic algal community. J. Mar. Res. 39: 749–765. Carrell, C. 1998. Water quality of three north Jamaican rivers and related reef health. B.S. Thesis, Baylor Univ. 74 p. Cochran, S. A. 1996. Geomorpholgy and biotic density of Dairy Bull Reef, Discovery Bay, Jamaica. B.S. Thesis, Baylor Univ. 101 p. Gaitros, A. M. 1996. Influence of biological and chemical variations on Jamaican reef health. M.S. Thesis, Baylor Univ. 131 p. Hughes, T. P. 1994. Catastrophes, phase shifts, and large scale degredation of a Caribbean coral reef. Science 265: 1547–1551. __________, B. D. Keller, J. B. C. Jackson and M. J. Boyle. 1985. Mass mortality of the echinoid Diadema antillarum Phillipi in Jamaica. Bull. Mar. Sci. 36: 377–384. __________, D. C. Reed and M. J. Boyle. 1987. Herbivory on coral reefs, Community structure following mass mortalities of sea urchins. J. Exp. Mar. Biol. Ecol. 113: 39–59. Jackson, J. B. C. 1997. Reefs since Columbus. Coral Reefs. 16-S: 23–32. Keller, B. D. 1983. Coexistence of sea urchins in seagrass meadows, An experimental analysis of competition and predation. Ecology 64: 1581–1589. Lessios, H. A. 1988. Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panama. Mar. Biol. 99: 515–526. ___________. 1995. Diadema antillarum 10 years after mass mortality, Still rare, despite help from a competitor. Proc. R. Soc. Lon. Ser. B. 259: 331–337. ___________, P. W. Glynn and D. R. Robertson. 1983. Mass mortalities of coral reef organisms. Science 222: 715. ___________, D. R. Robertson, J. D. Cubit. 1984. Spread of Diadema mass mortality through the Caribbean. Science 226: 335–337. Liddell, D. W. and S. L. Ohlhorst. 1987. Patterns of reef community structure, north Jamaica. Bull. Mar. Sci. 40: 311–329. Ogden J. C., R. A. Brown and N. Salesky. 1973. Grazing by the echinoid Diadema antillarum Philippi, Formation of halos around West Indian patch reefs. Science 182: 715–717. Perry, C. T. 1999. Reef framework preservation in four contrasting modern reef environments, Discovery Bay, Jamaica. J. Coast. Res. 15: 796–812. Sammarco, P. W. 1980. Diadema and its relationship to coral spat mortality, Grazing, competition, and biological disturbance. J. Exp. Mar. Biol. Ecol. 45: 245–272. _____________. 1982. Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J. Exp. Mar. Biol. Ecol. 65: 83–105. Woodley, J. D. 1999. Sea-urchins exert top-down control of macroalgae on Jamaican coral reefs I. Coral Reefs 18: 192. ____________, E. A. Chornesky, P. A. Clifford, J. B. C. Jackson, L. S. Kauffman, N. Knowlton, J. C. Lang, M. P. Pearson, J. W. Porter, M. C. Rooney, K. W. Rylaarsdam, V. J. Tunnicliffe, C. M. Wahle, J. L. Wulff, A. S. G. Curtis, M. D. Dallmeyer, B. P. Jupp, M. A. R. Koehl, J. Neigel, and E. M. Sides. 1981. Hurricane Allen’s impact on Jamaican coral reefs. Science 214: 749-755. ____________, P. M. H. Gayle and N. Judd. 1999. Sea-urchins exert top-down control of macroalgae on Jamaican coral reefs II. Coral Reefs 18: 193.

336


DATE SUBMITTED: March 7, 2000.

DATE ACCEPTED: December 11, 2000.

ADDRESSES: (C.S.M.) Department of Marine Geology and Geophysics, University of Miami, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, Florida 33149-1098. E-mail: . (R.M.B.) Department of Geology, Baylor University, P.O. Box 97354, Waco, Texas 76798-7354. E-mail: . CORRESPONDING AUTHOR (C.S.M), Tel: (305) 361-4812, x 3).