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271 J. Exp. Mar. Biol. Ecol., 1986, Vol. 95, pp. 271-278 Elsevier JEM 630 CHANGES IN BENTHIC COMMUNITY COMPOSITION FOLLOWING THE MASS MORTALITY OF DZADEMA AT JAMAICA’ W. DAVID LIDDELL Department of Geology and Ecology Center, Utah State University, Logan, UT84322-0705, U.S.A. and SHARON L. OHLHORST ~e~ariment of Fisheries and Wild&e and Ecofogv Center. Utah State University~Logan, UT 84322-5200. U.S.A. (Received 5 August 1985; revision received 21 November 1985; accepted 25 November 1985) Abstract: The urchin, Diadema antillatum Philippi, is normally ubiquitous on Caribbean reefs and exerts an important control on benthic algal populations through its grazing activity. At Discovery Bay, Jamaica, the urchin was essentially eliminated from fore reef sites during August, 1983 by disease. Four IOO-m2sites located between 5 and 22 m on the fore reef were censused prior to and after the urchin mortality. At 15m, the urchin density declined from 6.6 to 0.0. rn-’ while bottom cover by noncrustose algae (mainly Dictyora species and filamentous red and green algal turf species) increased from 30.7 to 49.7% within 2 wk of the urchins’ death and by 4 months had increased to 72.3%, finally declining to 64.7% after 1 yr. This sharp increase in algal cover was achieved at the expense of other reef benthos, such as crustose coralline algae and clionid sponges. A similar pattern was found at the other depths. Depending upon the urchins’ ability to re-establish itself, this trend may have serious implications for the shallower (< 30 m) Jamaican reefs, which are still undergoing a succession with recruitment of many coral species following Hurricane Allen, in 1980. Key words: Diadema; mass mortality; Jamaica; reefs; urchins INTRoDUff TON The sea urchin Diadema antillantm Philippi is normally ubiquitous on shallow reefs throughout the Caribbean. The urchin is an important grazer on benthic algae (Sammarco, 1980,1982a,b; Carpenter, 1981) and, occasionally, coral tissue (Bak & van Eys, 1975) and is a major bioeroder of hard substrata (Hunter, 1977). Populations of the urchin suffered mass mortality throu~out the Caribbean during 1983 due to an unidentified waterborne pathogen (Lessios er al., 1984). This paper documents the changes which occurred in the benthic community over the range of 5 to 22 m on the fore reef following the Diudema mass mortality at Jamaica. ’ Contribution No. 351 from the Discovery Bay Marine Laboratory. 0022-0981/86/$03.50 0 1986 Elsevier Science Publishers B.V. (Biomedical Division) 212 W.DAVIDLiDDELLANDSHARONL,OHLHORST METHODS Censuses of urchin pop~ations and sessile benthic community composition, were conducted at 2-wk, Cmonth (15 m only) and I-yr intervals following the death of the urchin at sites which had been previously censused. Censuses were conducted within areas consisting of 100 m2 on the West Fore Reef in the vicinity of Discovery Bay, Jamaica (18°30’N:77020’W) at 5, 10, 15, and 22m. Deeper sites (l30m) were visually, but not quantitatively, surveyed after the urchin die-off as prior censusing indicated that Diadema was present in extremely low numbers (0.0 to 0.1 * m - ‘) (Liddell et al., 1984a) and likely to exert little effect on benthic algal populations at these depths. Sessile benthic populations were censused by a linear point intercept method which utilized a series of 10-m lines with points located every 20 cm (50 points per line) (Liddell et al., 1984a). 111 to 586 points (typically 500) were counted at each site. Urchins were counted within ten, 1 x 10-m strips at each site. RESULTS In August of 1982 urchin numbers varied between 6.6 to 14.0. m- ’ on the fore reef terrace, decreasing sharply with increasing depth ( - 0.987 Spearman’s rho, P < 0.05) (Table I, Fig. 1). With the exception of pompously low values at 22 m, noncrustose algal cover appeared to follow an opposite pattern (Table I, Fig. 2). The urchin mortality was first observed in the Discovery Bay area in early August of 1983 (J. D. Woodley, pers. comm.; Hughes et al., 1985) and by the end of August, when our post-mortality censuses were conducted, urchin numbers had declined to nearly zero at all sites (Table I, Fig. 1). Changes in the algal community occurred rapidly after the urchin mortality with total noncrustose algal cover at most sites at least doubling over August, 1982 values by the end of August, 1983. For example, at 5 m total noncrustose algal cover increased from 17.6 to 55.4%, at 10 m from 22.5 to 4X9%, at 15 m from 30.7 to 49.7% and at 22 m from 14.8 to 56.1 y0 (Table I, Fig. 2). At 30 m Diadema densities were very low (0.1. m- “) prior to the urchin’s mortality, while percent cover by noncrustose algae (31.8%) was much higher than at shallower sites with abund~t Diadema (Liddell et al., 1984a). Nonquantitative visual surveys of the 30-m site at 2 wk and 1 yr after the Diudema mortality suggest that no significant changes occurred in noncrustose algal abundance. This strongly suggests that the changes in algal abundance on the shallower reef were indeed due to the decline in Diudemu and not some additional external factor. At 15 m (the only site for which December, 1983 data are available) the increase in algal cover continued through December, 1983 and appeared to level-off or decrease somewhat after 1 yr (August, 1984) (Table I). As algal cover increased between the August 1982 and August 1983 censuses, significant (x2, P < 0.001) shifts occurred in the composition of the noncrustose algal community at all sites (Tables I and II). For most sites the initial (August, 1983 versus (6%) 0'0 P’LS (6’f) T’P (L’P) L’ZI (8'8)6'SP (L’S) I'IZ (S’L) S’ZZ (03) 2'6 (0’01) L.ZL (9.L)Z’LI (9‘9) vss (p'o)2'0 (CL) 1'62 (S’9) 9’LI (8'Z)6x1 WO (p'6)L’OE (9'1)5'11 (6’9) @PI 0'0 (L’P) S’L (6’S) L'6t7 (6'1)9'9 (Ed 0’0 (L'I)8.Z (IX) O'S (2’6) S’9f 0’0 (S’L) L'P9 (6'0 9'9 (O’S) 9’91 0’0 (Z’S) !Ya (o'S)o'P (o’s) Z’OI (L’O) s-2 (S'S)831 (6'8)O'PI (5’6) 2’82 0’0 (827) 6’9 (L.9)Z'EZ (VP) 0’8 E’ZL (f’l) 0’1 (631) I.95 (5'6)0'81 q z_m.owapqJo 'ON lOJO ae@! asolsnm”o~ Uw?!j3 ql!M qqqnJ sm!od 'ON ex%'J, S,WQ ae%p? a”!,[eJo3 aso,s”J3 XXI) :lK+#qAJ :aqs 3yluaq U! sasueq3 :(Sau!l (D’ZI) O’PZ P83"v (II) 8LS h!unurmo3 Z8 ‘%nv (O'S)SE1 Z83"V WS 1B uoysoduroo (1I)OSS Sahel) (01) 96p (O’S) SI I (exe1 (S)85Z f8 +w (07) SZI :p861-?3(j1 (8) 1OP f 8 .anv (8.2) 8’2 Z83"V (II)985 (P'9)P‘EI (S)S6Z (01) 11s f8 .a”V (Z.Z) I’P f8 -a ~JB sanp~ tu 01 (L'9)0'8Z t8 +nV (II) 5% ueam peuaf (6’8) I’EZ (S'LI)O'ZP (6)ESt 0’0 (9’1) E’Z (YZ)p’61 28 ‘%nv UJ SI sa%ewaxad (z) III q)!~ .E8 .Z”V pnpue~s (5) 595 u! suoy?!~ap P8 ‘%W ul zz .sasaqlualed I TIav~ W. DAVID 1’4 LIDDELL AND SHARON L. OHLHORST Ui- U- 12- 10- 3 m *- 5 cl 6- *- + 2- 0’ I 5 I I 15 10 22 DWHM Fig. 1. Abundance of Diudema anfilkuwn from 5-22 m during 1982 and 1983: values plotted are mean numbers of individuals counted in 10, 10-m long and l-m wide strips at each depth (see Table I); 957” confidence intervals are indicated by vertical bars; l , 1982; n , 1983. a0 4I SO- so- +i)7 6 8 4 40- 8. E JO- 0’ I 5 I 10 15 I 22 DEPTH M Fig. 2. Percent cover by noncrustose algae from 5-22 m during 1982, 1983 and 1984: values plotted are mean percentages of reef surface occupied by noncrustose algae at each depth (see Table I); 95 Y0 confidence intervals are indicated by vertical bars; l , 1982; n , 1983; A, 1984. URCHIN MORTALITY ON JAMAICAN REEFS 27s August, 1982) rapid increase in algal abundance was achieved primarily by noncrustose macroalgae (mainly Dictyota species) (Table II). The 5-m site is an exception in that a relatively larger proportion of the initial increase in algal cover was by lilamentous red and green “turf’ species (Table II). All sites showed significant (5, 10, and 22 m: x2, P < 0.001; 15 m: x2, P -=z0.05) changes in gross benthic community composition (corals, crustose coralline algae, rubble with Clionu, and filamentous and noncrustose macroalgae) which occurred between the August, 1982 and August, 1983 censuses. The increase in total nonc~stose algal abundance (expressed as percent of bottom cover) from a 14.8 to 30.7% range for the four sites in 1982 to a 45.9 to 56.1% range in 1983 and to a 57.4 to 72.7% range in 1984 was achieved at the expense of other reef benthos, most notably crustose coralline algae and clionid sponges, both of which decreased significantly (Mann-jitney U, P < 0.01) in abundance following the algal bloom (Table I). DISCUSSION Although the present study differs from those conducted at Jamaica by Sammarco (1980, 1982a,b) in location (respectively, fore reef sites between 5-22 m on the fringing reef versus patch reefs at 2-6 m in the back reef), urchin density (2.5-l3.9*m-2 for Diadema on the fore reef versus 7 1.O. m - 2 in the back reef) and dominant algal species, it is of interest to compare the results of a “natural” versus artificial manipulation of urchin herbivore densities. During Sammarco’s (1982a) whole reef manipulation of urchin density, reduction of Diudema density to 1.O’ m _ 2 resulted in a si~~~~t increase in mean algal biomass (g decalcified dry weight ~0.25 m-‘) from 1.38 (SD k 0.23) to 8.22 (SD + 2.29) after ~5 months and to 14.74 (SD = 15.52) after z 15 months (his Table III). Coral cover actually increased significantly from 36.0 to 48.0% after 15 months when Diadema was eliminated, although coral cover decreased si~i~c~tly over this time interval when the very abundant (25.5 f m-“) Ec~jnomet~a was also eliminated from his study site (Sammar~o, 1982a, his Fig. 5). After x 1 yr, the present study found algal percent cover to increase from two to four times at all sites, while changes in coral abundance are more difficult to define. Finally, the dominant macroalgae (Dictyotu species, Lobophoru, Halimeda) encountered on the fore reef by the present study are notably absent from the back reef patches examined by Sammarco. Hughes et al. (1985) provide a vivid description of the effect of the disease upon Diadema populations along the north coast of Jamaica and also present photo-transect data documenting changes in the noncrustose macroalgal population following the demise of Diudema at a 7-m site at Rio Bueno. This site is located z 5 km to the west of the West Fore Reef site described herein. What is most striking when comparing their data with that from the West Fore Reef is the considerably smaller increase in macroalgal abundance at the Rio Bueno site. At their 7-m site macroalgae occupied 3.0% of the bottom prior to the mortality event, increasing to 15% after z 1 yr (Hughes Site: 4.6 (4.1) & Graham. 0.0 37.4 (6.7) 15.7 (6.5) 27.8 (5.6) Montagne 0.2 (0.6) 3.7 (1.8) 1.5 (2.2) 0.9 (1.4) 0.7(1.0) 550(11) 4.5 (3.7) 1.7 (1.6) 6.8 (3.3) 3.7 (1.8) 28.2 (8.5) 578(11) II 401 (8) Aug. 83 Aug. 82 0.9 (1.4) 17.7 (10.5) 3.1 (4.9) 2.1 (2.1) 2.7 (2.4) 4.3 (2.5) 586(11) Aug. 83 17.5 (5.4) 0.2 (0.6) 3.7 (2.3) 1.4 (2.1) 2.9 (2.3) 22.5 (5.4) 511 (IO) 15 In 44.9 (6.6) 0.0 5.5 (1.5) 5.2 (2.7) 8.6 (3.0) 9.4 (4.9) 295 (5) Dec. 83 values are mean percentages 8.3 (3.5) 1.0 (1.3) 1.7 (1.6) 14.0 (4.3) 8.4 (4.4) 31.3 (5.5) 585(11) Aug. 84 with standard and Ceramium sp. (reds) and Cladopora sp. and others (greens) 22.3 (6.8) 0.0 2.6 (1.4) 1.0 (1.0) 4.5 (3.1) _ 1982-1984: 15.5 (6.3) 10 m algae) Aug. 82 (noncrustose Aug. 84 at Jamaica ’ Primarily Valonia sp., Caultvpa sp. and Sargassum sp. d Primarily Jania adherens Lamouroux, Centroceras c/avu/atum (C. Agardh) b Primarily H. goreaui Colinvaux Q Primarily D. divaricata Lamouroux. green turf 0.0 13.8 (4.9) 3.1 (3.1) brown Other macroalgae‘ Filamentous red and” “Encrusting” 0.0 0.0 Lobophora variegata (Lamouroux) Wormsley 1.5 (2.4) 0.0 Halimeda ~pp.~ 11.8 (6.2) 258(5, Aug. 83 0.6 (1.0) 496 (IO) 5m composition Aug. 82 community Month/year: No. points (no. lines): in benthic Dictyora spp.” Taxa Changes TABLE 13.2 (5.0) 0.0 0.2 (0.7) 0.4 (0.9) 0.2 (0.7) 0.7(1.0) 453 (9) Aug. 82 deviations 20.1 (16.1) 1.0 (1.3) 0.0 0.0 3.6 (0.1) 31.5 (2.6) Aug. 83 I I I (2) 22 m in parentheses. 8.0 (3.7) 5.7 (5.3) 0.0 12.1 (3.9) 9.9 (4.2) 21.6 (4.7) Aug. 84 263 (5) URCHIN MORTALITY ON JAMAICAN REEFS 277 et al., 1985, their Figure 5). At the 5 m West Fore Reef site noncrustose algal abundance increased to 46.7% after 1 yr (Table I). The 15-m and 22-m West Fore Reef sites also show similarly large increases in noncrustose macroalgal abundance (Table I). We suggest that the reason for this dichotomy between two nearby localities is increased herbivory by fish at Rio Bueno. Although we are not aware of published data which would allow the testing of this hypothesis, observations by workers who have spent considerable time at both Rio Bueno and West Fore Reef sites indicate that fish are much more abundant at Rio Bueno (J. B. C. Jackson, pers. comm.). If the differences in algal abundance at the two localities are, indeed, due to differences in fish grazing pressure, this implies that many of the species contributing to the increase in algal abundance following the mass mortality of Diudema (Table II) do not possess strong defenses against fish grazing. The long-term effect of the urchin mortality and subsequent increase in algal numbers is uncertain and will depend largely upon the urchin’s ability to re-establish itself upon the reefs and its future resistance to the disease. Although scattered remnant populations of the urchin do exist in the Discovery Bay area, principally in near crest and backreef areas, no recolonization of our study sites had occurred as of August, 1984. After 12 yr urchin numbers are still very low (M. E. Hay, pers. comm.), in an area in which Diudema was removed at St. Croix in 1972 (Ogden et al., 1973), suggesting that Diudemu may be slow to recolonize reef habitats. The effects of the urchin die-off may be particularly severe at Jamaica as compared to other Caribbean sites for two reasons. Firstly, the Jamaican reefs are heavily overfished (Woodley, 1979), perhaps resulting in undue emphasis on Diudemu as a regulator of algal populations (Hay, 1984), although several of the abundant macroalgal species (e.g. Dictyotu, Lobophoru and Cuulerpu) are those which may exhibit some resistance to grazing by the main herbivorous fish groups (Morrison, 1984). Secondly, the shallow (< 30 m) Jamaican reefs are undergoing a succession following the 1980 Hurricane Allen (Woodley et al., 1981; Liddell et al., 1984b). Small, z 5 cm in height, coral recruits (most notably Acroporu pulmatu (Lamarck) at 5 m and A. cervicomis (Lamarck) at 15 m, both of which were apparently derived from larval settlement) were observed in our study sites by early August, 1983, although they were not yet abundant enough to be recorded by the transects. Small corals are typically inferior competitors with algae (Birkeland, 1977) and may be expected to show high mortality following the algal bloom. Our observations suggest that this is indeed the case. Such mass die-offs of urchins are known from additional localities throughout the Caribbean (summary by Lessios et al., 1984) as well as the Mediterranean (Boudouresque et al., 1981; Azzolinaet al., 1983; Maes, 1983), California (Pearse et al., 1977; Pearse & Hines, 1979) and Nova Scotia (Miller & Colodey, 1983; Scheibling & Stephenson, 1984). Considering the important role of urchins as regulators of benthic communities and the apparent ubiquity of urchin mass mortality, further study of the ecological consequences of such mass mortality events, including the long-term monitoring of areas so affected, is potentially of great importance. 278 W. DAVID LIDDELL AND SHARON L. OHLHORST ACKNOWLEDGEMENTS We wish to thank S. K. Boss (Utah State University), S. A. Kohut (University of New Orleans), and I. M. Sandeman @rent University) for their assistance in reef censuses. Also, C. J. Slocum (Stockton College) for assistance in identification of filamentous algae. REFERENCES AZZOLINA,J. F., C. F. BOUDOURESQUE & H. NEDELEC,1983. Dynamique des populations de Paracentrotus lividus (Lmk.) (Echinidae) dam la Baie de Port-Cros (Var, France). Symbioses, Vol. 15, pp. 212-213. BAK, R. P. M. & G. VANEYS, 1975. Predation of the sea urchin Diadema antillunrm Philippi on living corals. Oecologia (Berlin), Vol. 20, pp. 11i-l 15. BIRKELAND,C., 1977. The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. Rroc. Third Int. Coral Reef Symp., Rosenstiel School, University of Miami, Miami, Fla., Vol. 1, pp. 15-21. BOUDOURESQUE, C. F., N. NEDELEC& S. A. SHEPHERD,1981. The decline of a population of the sea urchin Paracentrotus lividus in the Bay of Port-Cros (Var, France). Rapp. Comm. Int. Mer Medit., Vol. 27, pp. 233-244. CARPENTER,R.C., 198l.Grazing by Diadema antillarum (Philippi) and its effects on the benthic algal community. J. Mar. Res., Vol. 39, pp. 749-765. HAY, M. E., 1984. Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical? Ecofow, Vol. 65, pp. 446-454. HUGHES, T.P., B.D. KELLER, J.B.C. JACKSON& M.J. BOYLE, 1985. Mass mortality of the echinoid Diadema antillarum Philippi in Jamaica. Bull. Mar. Sci., Vol. 36, pp. 377-384. HUNTER, I. G., 1977. Sediment production by Diadema ant&rum on a Barbados fringing reef. Proc. Third Int. Coral ReefSymp.,Rosenstiel School, University of Miami, Miami, Fla., Vol. 2, pp. 105-I 10. LESSIOS, H. A., D. R. ROBERTSON& J. D. CUBIT, 1984. Spread of Diadema mass mortality through the Caribbean. Science, Vol. 226, pp. 335-337. LIDDELL,W.D., S.L. OHLHORST& S.K. BOSS, 1984a. Community patterns on the Jamaican fore reef (15-56 m). Puleont. Am., No. 54, pp. 385-389. LIDDELL,W. D., S.L. OHLHORST& S. K. Boss, 1984b. Community patterns on a Jamaican fringing reef: 1976-1983. Adv. in Reef Sci. Mtg., Miami, Fla., Abstracts, pp. 69-70. MAES, P., 1983. Etude biopathologique des lesions tegumentaires chez les oursins reguliers littoraux. Symbioses, Vol. 15, pp. 237-238. MILLER,R. J. & A. G. COLODEY,1983. Widespread mass mortalities of the green sea urchin in Nova Scotia, Canada. Mar. BioL, Vol. 73, pp. 263-267. MORRISON,D., 1984. Chemical defenses in coral reef macroalgae: effectiveness against different herbivore types. Abstracts Bull. Ecol. Sot. Am., Vol. 65, p. 71. OGDEN, J.C., R.A. BROWN& NSALESKY, 1973. Grazing by the echinoid Diadema antiilarum Philippi: formation of halos around West Indian patch reefs. Science, Vol. 182, pp. 715-717. PEARSE,J. S., D.P. COSTA,M.B. YELLIN& C.R. AEGIAN, 1977. Localized mass mortality of red sea urchins, Stron~loceniroius Franciscans, near Santa Cruz, California. Fish. Bull. NOAA, Vol. 75, pp. 645-648. PEARSE,J. S. & A. J. HINES, 1979. Expansion of a central California kelp forest following the mass mortality of sea urchins. Mar. BioL, Vol. 51, pp. 83-91. SAMMARCO,P. W., 1980. Diadema and its relationship to coral spat mortality: grazing, competition, and biological disturbance. J. Exp. Mar. Biol. Ecol., Vol. 45, pp. 245-272. SAMMARCO, P.W., 1982a. Echinoid grazing as a structuring force in coral communities: whole reef manipulations. J. Exp. Mar. Bioi. Eeol., Vol. 61, pp. 31-55. SAMMARCO,P. W., 1982b. Effects of grazing by Diudema antiZ~u~mPhilippi (~chinode~ata : Echinoidea) on algal diversity and community structure. J. Exp. Mar. Biol. Ecol., Vol. 65, pp. 83-105. SCHEIBLING, R.E. & R.L. STEPHENSON, 1984. Mass mortality of Strongylocentrotus droebachiensis (Echinodermata: Echinoidea) off Nova Scotia Canada. Mar. Biol., Vol. 78, pp. 153-164. WOODLEY, J. D., 1979. The effects of trap-fishing on reef communities in Jamaica. Proc. Thirteenth Mtg. Assoc. qf Island Marine Laboratories of the Caribbean, Abstracts, p. 27. WOODLEY,J.D. et al., 1981. Hurricane Allen’s impact on Jamaican coral reefs. Science, Vol. 214, pp. 749-755.