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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%)
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W. DAVID
1’4
LIDDELL
AND SHARON
L. OHLHORST
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m
*-
5
cl
6-
*-
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2-
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I
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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.
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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.
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