J. Exp. niiar. B&l. Ecol., 1987, Vol. 113, pp. 39-59
39
Elsevier
JEM 00960
Herbivory on coral reefs: community structure following
mass mortalities of sea urchins
Terence P. Hughes, Daniel C. Reed and Mary-Jo Boyle
Department ~~3i~l~~~al Sciences, university of Ca~~~~~. Santa Barbara, California, U.S.
(Received 20 March 1987; revision received 12 May 1987; accepted 15 July 1987)
Abstract: The community structure of Jamaican coral reefs has undergone drastic change since mass
mortalities ofthe long-spined black sea urchin Diadema anrillarum Philippi occurred in 1983. In the absence
of Diadema, algal abundance has increased enormously, up to a mean of 95% cover or 4.6 kg wet
weight m-a. Coral cover, which was already low on some reefs following Hurricane Allen in 1980, has been
further reduced by as much as 60% since 1983 by competition with algae. Densities of D. antillurum at 10
sites in 1986 ranged from 0 to 12% of pre-1983 levels. Other echinoids, which might potentially compensate
for the lack of herbivory from D. anfillarum, have not increased significantly in density. Numbers of
herbivorous scarids and acanthurids also remain at relatively low levels, because of overfishing. In the
absence of high densities of fish and sea urchins, it is likely that recent changes in community structure will
continue, resulting in further replacement of corals by algae in shallow water. The impact of the urchin mass
mortalities is qualitatively similar to previous experimental removats of this species. In both cases, removal
of echinoids resulted in substantial increases in macroalgae. However, quantitatively, the responses of algaI
and coral communities to the natural die-off were signiticantiy greater, probably due to wide differences in
spatial and temporal scales of the respective perturbations.
Key words: Herbivory; Coral reef; Alga; Diadema antillarum
INTRODUCTION
A major question in community ecology is how interactions between species influence
their distribution and abundance. On tropical reefs, the abundance of algae is often
maintained at low levels because of herbivory (e.g., Sammarco, 1977, 1982a,b; Ogden
& Lobel, 1978; Hay etai., 1983; Hay, 1985; Carpenter, 1986; Lewis, 1986). Consequently, substrates that are protected experimentally from grazing rapidly become
colonized by macroalgae (Ogden et al., 1973a,b; Sammarco et al., 1974; Vine, 1974;
Wanders, 1977; Borowitzka, 1981; Carpenter, 1981; Sammarco, 1983; Hay&Taylor,
1985) which in turn inhibit recruitment and growth of corals (Birkeland, 1977; Potts,
1977; Bak & Engel, 1979; Sammarco, 1980; Lewis, 1986). Furthermore, algal biomass
is often high where herbivores are naturally scarce, e.g., on many highly turbulent reefs
or reef flats (Wanders, 1976; Adey et al., 1977; Connor dc Adey, 1977; Hay, 1984; Adey
Publication 394 of the Discovery Bay Marine Laboratory.
Correspondence address: T. P. Hughes, Department of Biological Sciences, University of California,
Santa Barbara, CA 93106, U.S.
OO2~-0981~87~SO3.50
% 1987 Elsevier Science Publishers B.V. (Biomedical Division)
40
T. P. HUGHES
ETAL.
& Steneck, 1985; Lewis, 1986), or within the territories of pomacentrid damselfish (e.g.,
Brawley & Adey, 1977; Williams, 1979; Lobel, 1980; Sammarco, 1983).
This paper examines herbivore-algal-coral
interactions on Jamaican reefs, revealed
by unprecedented mass mortalities of the long-spined black sea urchin Diadema
antillarum Philippi. Mass mortalities of D. antillarum occurred throughout the
Caribbean and tropical western Atlantic in 1983-84 (Bak et al., 1984; Lessios et al.,
1984a,b; Hughes et af., 1985; Hunte et al., 1986). Other species of echinoid were
unharmed (Bak et al., 1984; Lessios et al., 1984b; Hughes et al., 1985), indicating that
the mortalities were caused by an unidentified species-specific pathogen. Population
densities of D. antilLa~m on Caribbean coral reefs were drastic~ly reduced: e.g., by
X7-100% in Barbados (Hunte eta& 1986), 97-100% in Curaqao (Bak et al., 1984),
98-100x in Jamaica (Hughes et al., 19851, 94-992 in Panama (Lessios et al., 1984),
and by >99% in St. John (Levitan, in press).
D. antiflarum is a major herbivore on Caribbean reefs (e.g., Lewis, 1964; Randall
etal., 1964; Ogden etal., 1973a,b; Sammarco et al., 1974; Ogden & Lobel, 1978;
Carpenter, 1981, 1986; Sammarco, 1982a,b; Hay & Taylor, 1985). Its feeding activities
have been shown to influence recruitment in corals (Sammarco, 1980), and cause
substantial bioerosion (Hunter, 1977; Ogden, 1977; Scot% et al., 1980). In the first few
weeks and months after the demise of D. antillapum, there was a predictable increase
in abundance of algae (Carpenter, 1985; Hughes, 1985; Hughes et al., 1985; Liddell &
Ohlhorst, 1986). Here, we examine over a longer time scale the changes in reef
community structure that have occurred > 3 yr after the sea urchin die-off.
The low densities of echinoids following the mass mortalities provide an unusual
opportunity to observe some of the effects of reduced levels of herbivory on reef
communities. Although we cannot prove that recent increases in macroalgal biomass
were caused by the sea urchin die-off, we offer the following evidence as strong support
for this hypothesis. First, experimental removal of D. antillarum before the mass
mortalities (Ogden et al., 1973b; Sammarco, 1980, 1982a,b; Sammarco et al., 1974;
Carpenter, 1981, 1986; Hay 8c Taylor, 1985) resulted in increases in algal abundance
and a sequence of change in species composition very similar to those following the
die-off (Carpenter, 1986; Liddell & Ohlhorst, 1986). Secondly, both an urchin die-off
and a sustained algal bloom are unprecedented in three decades of intensive research
in the vicinity of Discovery Bay, Jamaica. Seasonal changes in algal abundance are
typically < 10-20x (Carpenter, 1981; Hughes, unpubl. data), in marked contrast to
recent events. A short-lived bloom did occur for a few weeks following Hurricane Allen
in 1980, when forereef populations of Diadema on exposed reefs were briefly depressed
(Woodley et al., 1981). By 1981, numbers of Diadema had fully rebounded, and the
abundance of algae was again reduced (Hughes et al., 1985). Thirdly, large increases
in algal biomass have occurred following the die-off on other Caribbean reefs where
Diadema was formerly abundant (e.g., St Croix, see Carpenter, 1985,1986). In contrast,
there has been relatively little change in algal communities on reefs where D. anti~la~m
was always comp~atively rare (even before the mass mortalities took place), and where
41
HERBIVORY ON CORAL REEFS
other herbivores continue to graze heavily (e.g., San Blas Is., Panama; T.P,Hughes,
pers. obs.).
We show here that densities of D. ~nti~~~~rnin 1986 remain very low compared with
levels before the die-off in 1983. Recent recruitment, indicated by the presence of small
Diudema, was detected at only a few sites. Other echinoid species have not increased
substantially in abundance. Algal biomass and cover has continued to rise throughout
the past 3 yr to some of the highest levels recorded for coral reefs, while coral cover has
sharply declined.
STUDY SITES AND
METHODS
The abundance of D. ~~t~l~a~rn,algae, and corals was measured in 1986 at nine sites
that were chosen because: (1) they represented a wide variety of habitats formerly
inhabited by D. antillancm; and (2) estimates of the abundance of D. antillarum and of
algae prior to the urchin die-off in 1983 were available. Three of the sites were in the
shallow (l-3 m deep) backreef of Discovery Bay (Crosby Patch Reef, Stills Patch Reef,
and the Inner Reef Crest), three were on nearby forereefs (2-3 m and 10 m on Mooring
1 Reef, and 20 m on Dancing Lady Reef), and three were at Rio Bueno (on a shallow
platform at 7 m, and on a nearby vertical wall at 10 and 20 m), 5 km west of Discovery
Bay (see Fig. 1 for site locations).
DIADEMA ABUNDANCE
A survey for the presence of Diadema was conducted in August and September 1986
at the nine sites listed above, and at Pear Tree Bottom (7 km east of Discovery Bay),
CARIBBEAN
SEA
D/SCO,‘ER,’
BAY
-1
1OOkm
Fig. 1. Map of Jamaica showing sites investigated (see text for brief site descriptions). A, Crosby and Stills
Patch Reefs; B, Inner Reef Crest; C, forereef; D, Rio Bueno.
42
T. P. HUGHES
ETAL.
where censuses had been made before and immediately after the urchin die-off
(Carpenter, 198 1; Sammarco, 1982a, b; Karlson, 1983; Hughes et al., 1985). On reefs
where Diadema were present, densities were estimated from 20 haphazardly positioned
l-m* quadrats. At the same time, we measured densities of four other species of urchin
that were encountered, Echinometra viridis Agassiz, Eucidaris tribuloides (Lamarck),
Lytechinus williamsi Chesher, and Tnjmeustes ventricosus (Lamarck).
To learn more about the dynamics of the surviving Diadema populations, we
measured maximum test diameters where sufftcient urchins could be found (i.e., at Rio
Bueno, and the backreef of Discovery Bay). Data from Crosby and Stills Reefs were
combined to form a joint patchreef sample. All Diadema that were encountered were
measured in situ using modified calipers with extended jaws. Sample sizes ranged from
49 to 70 individuals per site.
ABUNDANCE
OF ALGAE AND CORALS
At each of the nine sites, ten 10-m long transects were laid out haphazardly, and the
percent cover of sessile animals and algae was estimated by counting the number of
centimeters of tape measure that covered each taxon. Additional data on percent cover
of corals and macroalgae at Rio Bueno were obtained by planimetry of color slides, of
a belt transect (16 mz at 7 m depth) which has been photographed regularly since July
1983 (Hughes et al., 1985), and of 16 l-m* quadrats on a vertical wall at depths of
lo-20 m that have been monitored annually for up to 10 yr (Hughes, 1985, and
references therein).
Algal biomass at the nine sites was measured as wet weight, dry weight, and
decalcified dry weight. These three standard measures allow comparison with previous
tropical studies (e..g, wet weight: Doty, 1971; Sammarco et al., 1974; Adey et al., 1977;
Brawley & Adey, 1977; Connor & Adey, 1977; dry weight: Wanders, 1976; 1977;
Lobel, 1980; Borowitzka, 198 1; De Ruyter van Steveninck & Breeman, 198 1; Vooren,
198 1; Hatcher & Rimmer 1985; Levitan, in press; decalcified dry weight: Vine, 1974;
Carpenter, 1981, 1986; Sammarco, 1982a, 1983). Crustose coralline algae were rarely
encountered in 1986, and are excluded from our analyses. Algal samples were gathered
within 15 10 x IO-cm quadrats at each site by collecting the entire substratum if
possible, and removing all attached algae in the laboratory, or by scraping off and
picking all the epibenthic algae in situ. The quadrats were positioned at regular
predetermined intervals along the transects used to measure percent cover (five each
at the midpoint, 3- and 6-m mark). Many of the quadrats were partially filled by corals
or sponges, and the algal biomass in some of our samples was close to 0. Algae (n = 135
samples) were sorted in the laboratory into tilamentous, foliose, and calcified fractions,
identified to family or genus, and spun in a salad spinner to remove excess water for
wet weighing. Samples were then ovendried at z 45 oC for 24-48 h, and weighed again.
Finally, the algae were decalcified with a 5% acid solution, dried, and weighed a third
time.
43
HERBIVORYON CORALRE FS
RESULTS
DIADEMA
The pattern of distribution and abundance of Diadema antillantm was altered
drastically by the mass mortalities in 1983 (Hughes et al., 1985; Liddell & Ohlhorst,
1986), and there has been little change > 3 yr later (Table I). Prior to the die-off, the
highest densities of D. ~ntill~~rn were found on Crosby and Stills Patch Reefs in the
backreef (up to a mean of 71. m - ‘; Sammarco, 1982a,b). On the forereef and at Rio
Bueno, abundances in shallow water were typically z 10 - m - ‘, and generally declined
with increasing depth (Table I; see also Liddell & Ohlhorst, 1986). In September 1986,
we could not find any Diadema after extensive searching at six sites for which prior data
are available (Table I). Elsewhere, the three backreef areas and 7-m depth at Rio Bueno
had l-9% of former densities. At 10 m on the vertical wall at Rio Bueno, densities have
increased significantly during the 3 yr since the mass mortality occurred, but only to
12% of levels before 1983 (Mann-Whitney test, P < 0.005). Other vertical walls at Pear
Tree Bottom and all fore-reef sites had no Diadema (i.e., fewer than one urchin per hour
of searching per diver) below a depth of l-3 m.
TABLE I
Densities of II. anfillarum (mean no. . m - 2 f SD) before and after the die-off at 12 sites (see Fig. 1 for site
locations). No. of mz sampled are shown in parentheses. * Before data from 1982 and 1983 at Rio Bueno,
Dancing Lady, and Pear Tree Bottom (Hughes ef al., 1985), 1978 at Mooring 1 (Carpenter, 1981), 1976-78
at the Inner Reef Crest (Karlson, 1983), and from 1973 at Crosby and Stills Patch Reefs (Sammarco, 1982a).
Zero densities in 1986 were determined by whole-reef surveys. Densities of Diudema before and after the
die-off were significantly different at all sites (at the 0.001 level, Mann-Whitney U test or Krustah-Wallis
test).
Site
Depth
(m)
After die-off
Before die-off+
September 1983
September 1986
Rackreefs
Inner Reef Crest
Crosby Patch Reef
Stills Patch Reef
lm
2m
2m
0.35 + 0.55 (20)
0.80 * 1.01 (20)
0.35 * 0.75 (20)
3.9 f 7.4 (116)
71.0 + 19.5 (8)
33.5 f 16.7 (8)
Forereefs
Dancing Lady
Mooring 1
Pear Tree Bottom
lpio Buena
8m
15m
3m
10.5 m
10 m
10.5 5
4.7 +
8.1 f
12.2 f
8.9 f
7.2 (20)
2.4 (20)
0.7(33)
4.3 (17)
5.5 (21)
0.05 f 0.22 (20)
0
(20)
7m
10m
20 m
11.7 + 7.6(16)
3.5 * 7.3 (66)
0.7 + 0.8 (6)
0.15 f 0.25 (16)
0.08 f 0.10 (66)
0
(20)
0
(20)
0
0
0
0
0
0.15 & 0.37 (20)
0.45 & 0.71 (40)
0
44
T.P. HUGHES ETAL.
The Diudema population at Rio Bueno in 1986 consisted entirely of very large urchins,
with a mean test diameter of 68 mm (Fig. 2). In contrast, on Crosby and Stills Patch
Reefs and on the Inner Reef Crest, individuals were smaller, with mean sizes of 57 and
5 1 mm, respectively (Kruskall-Wallis test, P < 0.001). Moreover, the bimodal distribution of test diameters from the backreef sites indicates the presence of young as well
as older cohorts. Thus, these size frequencies indicate that some recruitment has
occurred recently in the backreef, but not at Rio Bueno where juveniles are absent (or
at the three forereef sites, where there are virtually no Diudema of any size).
Fig. 2. Size-frequency distribution of maximum test diameter of D. anfillurum in September 1986, at 7 m
depth at Rio Bueno, and Inner Reef Crest, Crosby and Stills Patch Reefs. Sample sizes range from 49 to
70 urchins.
OTHER URCHIN SPECIES
Three years after the mass mortality of Diadema, there apparently has been no
substantial increase in the population densities of sympatric echinoid species that
survived the 1983 die-off unharmed. Densities of Echinometra viridis, Eucidarik
tribuloides, and Lytechinus williamsi were measured in 1973-75 on Crosby and Stills
Patch Reefs by Sammarco (1982a). The combined density of these species over this
period ranged from 24 to 29 * m - ’ on Crosby and from 3 1 to 54. m - ’ on Stills (Table II
in Sammarco, 1982a). Densities of D. antillanrm were about twice those of all other
echinoids combined on Crosby Reef, and roughly equal on Stills Reef (Sammarco’s
data in Table II). Renewed censuses, using identical techniques in 1986, failed to show
any dramatic rise in numbers of other echinoids on these two patch reefs which might
compensate for the lack of Diudema (Table II). The most abundant species, Echinometru
HERBIVORY
ON CORAL REEFS
45
Rio Bueno
Forereef
Mooring 1
Mooring 1
Dancing Lady
Inner Reef Crest
Crosby Patch Reef
Stills Patch Reef
Backreef
Site
20 m
10m
7m
2-3 m
10m
20m
lm
2m
2m
Depth
(m)
< 1%
< 1%
~2%
< 2%
_
cover
cover
cover
cover
by
by
by
by
noncrustose
macroalgae
noncrustose
macroalgae
algae ( 1977)5
( 1983)4
algae ( 1977)5
( 1983)4
3% cover by macroalgae (1983)’
22% cover by noncrustose algae (1978)3
40% cover by noncrustose algae (1978)3
34g wet rn-’ (1974)’
2.38 kg wet m - z (1974)’
6-29 g decal. m - ’ ( 1973-75)2
5.5 g decal. m-’ (1973)’
Before die-off* (date)
9 1% cover
87% cover
72% cover
13% cover
8 1% cover
15% cover
by
by
by
by
by
by
noncrustose
macroalgae
noncrustose
macroalgae
noncrustose
macroalgae
algae (Table V)
(Fig. 5)
algae (Table V)
(Fig. 5)
algae (Table V)
(Fig. 5)
95% cover by noncrustose algae (Table V)
94% cover by noncrustose algae (Table V)
1.79 kg wet m - ’ (Table IV)
4.55 kg wet m ._2 (Table IV)
196 g decal. m-* (Table IV)
228 g decal. ma2 (Table IV)
ARer die-off (September 1986)
Summary of algal abundance. All biomass estimates are per m*. Statistical tests between all sets of observations are not possible because of different
methodoio~es. For all sites combined, there was a significant increase in algae following the die-off (P = 0.002, sign test). Sources: (1) Brawley & Adey (1977);
(2) Sammarco (1982a); (3) Carpenter (1981); (4) present study, macroalgae defined as those species large enough to be seen in photographs of long-term
quadrats; (5) transect data in Hughes & Jackson (1985), includes both macroalgae and smaller turfs.
TABLE III
G
3
z
-I
Y
HERBIVORY
ON CORAL
REEFS
41
viridis, actually declined significantly on both Crosby and Stills Reefs (t test, P < 0.05
and P < 0.001, respectively). Lytechinus williamsiincreased slightly on Crosby (t test,
P -C O.OOl), but remained steady on Stills (Table II). Eucidaris tribuloides showed no
significant change in abundance on either reef. A fifth echinoid species, Tripneustes
ventrikosus (rarely encountered by P.W. Sammarco, pers. comm.), was also present at
very low levels in 1986. Overall, total echinoid densities in 1986 were < 20% of earlier
estimates (P < 0.001, Table II).
ALGAL
ABUNDANCE
Following the die-off, there was a dramatic increase in algal abundance at all study
sites (sign test, P = 0.002, Table III; Fig. 3). The mean biomass of epibenthic (noncrustose) algae was B 500 g wet weight. m - 2, almost everywhere we examined
(Table IV), and algal percent cover was typically 85-95 % (Table V). Algal composition
varied widely from reef to reef (Fig. 4). We compare below the current abundance of
algae with previous measurements from Discovery Bay backreefs and forereefs, and we
describe the time course of the algal bloom at Rio Bueno.
Backreefs
On Crosby Patch Reef, Sammarco (1982a) estimated that in the presence of large
numbers of Diadema antillarum the algal biomass ranged (nonsignificantly) from 6 to
29 g decalcified dry weight * m-’ during 1973-75. The amount in September 1986 was
nearly seven times greater (Table II). On Stills Patch Reef, following the experimental
removal of D. antillarum, algal biomass in 1973 increased over 18 months from 5.5 to
60 g decalcified dry weight .rnw2 (Sammarco, 1982a). The amount of algae on Stills
Reef 38 months after the die-off was nearly four times greater than the highest levels
seen after the experimental removals (Table II). Most of the algae on the patch reefs
in 1986 were filamentous (Fig. 4), primarily Gelidiaceae, Ceramiaceae, and
Acanthophora specifera (Vahl). Algal cover was almost complete (Table V), and was
typically > 10 cm thick.
On the Inner Reef Crest, Brawley & Adey (1977) found a high algal abundance,
averaging 2.38 kg wet weight * rnp2, in 1974. This is by far the greatest previous estimate
of algal biomass from Jamaican reefs, in large part because of the presence of many
damselfish gardens, principly Stegastes planifrons and S. dorsopunicans (Brawley &
Adey, 1977). Following the urchin mass mortalities, the algal abundance on the Inner
Reef Crest has doubled (Table III). Most of the algae were filarnentous Gelidiaceae or
erect calcified Halimeda species (Fig. 4).
Forereefs
The percent cover of algae at 2-3 m on the forereef (Mooring 1 Reef) averaged 95 %
in 1986 (Table V), but the biomass was the lowest we found (Table IV) because most
of the algae were small filaments (Fig. 4). They appeared to be heavily grazed by fish,
48
T. P. HUGHES
ETAL.
HERBIVORY ON CORAL REEFS
49
BACKREEF
P
FOREREEF
E
0
i
8
FILAMENTS
FOLIOSE
CALCIFIED
Fig. 4. Algal composition with respect to biomass (decalcified dry weight) at the nine study sites.
TABLE
IV
Algal biomass at nine sites in September 1986, expressed as wet weight, dry weight, and decalcitied dry
weight. All values are g m _ ‘, mean _+SE, based on samples from 15 random 100-cm* quadrats per site.
Backreef
Inner Reef Crest
Crosby Patch Reef
Stills Patch Reef
4554 + 802
1730 * 388
422 & 82
2352 + 733
435 f 89
196 f 45
1212 + 215
313 + 54
228 & 43
Wet weight
Dry weight
Decalcified dry weight
--...
Forereef
Wet weight
Dry weight
Decalcified dry weight
_-_-
2m
10m
20m
439 I: 119
IlO*
39rt 11
3253 + 1020
1436 f 612
303 + 106
1791 + 391
846 k 232
186 + 51
-
Rio Bueno
~--
Wet weight
Dry weight
Decalcified dry weight
7m
IO m
4124 -t_1402
2280 F 847
496 + 208
~_
543 k 448
315 & 288
84 k 75
20 m
_.-...
500 + 217
230 + 116
41 + 26
50
T. P. HUGHES
ETAL.
that are more common on the shallow forereef than elsewhere (e.g., Hay, 1984; pers.
obs.). Calcareous crusts, which used to cover 20-30% of the bottom at this site
{Carpenter, 198 l), have been replaced almost entirely by tilamentous algal turfs (mostly
Ceramiaceae), and a smaller amount of foliose Dictyota species (Fig. 4). In contrast,
50 m seaward at a depth of 10 m, there were massive amounts of foliose algae, especially
Dictyota and Padina, and Halimedu species, with an average total wet weight of
> 3 kg. m - ’ (Table IV). Before the algal bloom, Carpenter (198 1) found negligible
amounts of foliose macroalgae at both the 2-3- and 10-m sites.
At 20 m on the forereef (Dancing Lady Reef) prior to the die-off of Diadema, Brawley
& Adey (1977) estimated that the biomass of epilithic (noncrustose) algae at 22 m,
outside territories of the three-spot damselfish Stegustesplanifons, was only 34 g wet
weight. m - 2. Within the territories, where herbivorous fish and Diadema are repelled
by the damsel~sh (e.g., Williams, 1979), the average biomass was 360 g ‘ m-‘, or 10
times greater. The average biomass of algae at 20 m on the same reef is now roughly
live and 50 times greater, respectively, than Brawley & Adey’s (1977) estimates inside
TABLE V
Mean percent cover (_+ 1 SE) of sessile organisms and sand in September
1986 at nine study sites. Algae
includes both macro aIgae and turfs. See Fig. 5 for cover of macroalgae only at Rio Bueno. Data based on
10 10-m transect per site.
Backreef
~.Inner Reef Crest
Afgae
Hard corals
Soft corals
Sponge
Sand
Crosby
Patch
94.2
2.6
3.2
0.2
87.3 + 9.2
0.1 * 0.2
0
0
13.6 I 11.0
f
f
t
*
0
5.0
2.1
4.2
0.4
Reef
Stills Patch
I~
94.6
2.3
3.0
0.4
Reef
& 2.0
F 1.5
* 1.7
& 0.9
0
Forereef
Algae
Hard corals
Soft corals
Sponge
Sand
2m
10m
95.2 rt 4.2
2.0 $ 1.8
2.6 f 2.3
0
0.1 * 0.3
93.9 2 4.5
5.8 & 2.1
0.3 + 0.3
0
0
20 m
86.2
7.0
0.4
1.2
5.2
+ 8.2
+ 4.2
& 0.4
& 1.6
t 6.4
Rio Bueno
7m
10m
Algae
Hard corals
Soft corals
Sponge
Sand
_.
90.6 k
8.2 i:
1.2 +
0
0
4.1
3.9
2.2
72.4
23.9
3.4
0.3
k 2.8
& 3.4
* 2.0
+ 0.7
0
20 m
.-.___I_
80.9
13.1
1.5
4.5
+
i
rt
i
0
9.3
7.5
2.3
2.9
51
HERBIVORY ON CORAL REEFS
and outside of damselfish territories (Table III). Before the urchin die-off, the heavily
grazed algal communities outside pomacentrid territories consisted almost entirely of
crustose corallines and a few tufts of calcified Halimeda in contrast to the algal turfs
and occasional foliose species that formed the relatively lush damselfish gardens
(Brawley & Adey, 1977). By 1986, the spatial pattern of algal abundance has been
reversed. Damsel&h continue to defend their gardens, but now there is clearly less algal
biomass within their territories than outside because most of the algae inside continue
to be lilamentous turfs, while algal communities outside now cover > 90% of the
substratum (Table V) and are composed of a variety of larger foliose and erect calcified
species, primarily ~~ctyota, P~dina, ~obo~~or~, and Ha~i~eda (Fig. 4).
Rio Bueno
The percent cover of algae, excluding calcareous crusts, at all depths examined at Rio
Bueno prior to the urchin die-off was very low, typically l-3% (Fig. 5). Over the past
3.5 yr, cover by macroalgae at 7-20 m has risen lo-fold. The increase has been most
dramatic at 7 m, from 2.5x, 1 wk before the mass mortalities, to almost 90% cover,
ALGAL
:
(9
;1
COVER,
1983 - 1986
80
60
k
5
W
JUL 83
tg
JAN84
f-1
JUN 84
CII
I-:]
[:-I
JAN85
JUN 85
JAN 8 6
i_?
SEP 86
40
B
z
20
0
7m
IOm
15m
20m
Fig. 5. Macroalgal cover vs. time (mean f SE) at 7,10,15, and 20 m depths at Rio Bueno, from the month
before the die-off of L?.~~rjZ~u~~ (July 1983) to September 1986.
primarily by L)ictyota species, in September 1986. ~aZ~~ed~ accounted for most of the
decalcified biomass at all depths (Fig. 4). The decline in algal abundance below 7 m may
be due in part to the sudden change in reef topography from a shallow platform at 7 m
to a vertical wall. On more gently sloping forereefs at Discovery Bay, there were
substantially more algae in 1986 at 10 and 20 m than at the same depths at Rio Bueno
(Tables IV, V).
T. P. HUGHES ET&.
52
CORAL ABUNDANCE
The algal bloom has coincided with a significant reduction in the abundance of corals
since 1983, especially in shallow water. On the backreef, Crosby and Stills Patch Reefs
had only 2-3% cover by corals in 1986, compared with up to nearly 50% from 1973-75
before the die-off of D. antillamm (Sammarco, 1982a). The patch reefs incurred very
limited damage from Hurricane Allen in 1980 (Woodley et al., 1981; T.P. Hughes, pers.
obs.), By 1986, many corals were partially or completely covered by dense growths of
filamentous algae. Dead elkhorn and staghom corals were well preserved and still
intact, indicating that mortality was very recent and not caused by physical destruction
during the hur~c~e. On the Inner Reef Crest, coral cover in 1986 was virtually 0, and
cover by zooanthids has declined sharply from I1 y0 in January 1984 (Karlson, in
review) to almost 0 (Table V).
Coral cover on the Discovery Bay forereefs is at the lowest levels ever recorded there.
The Acrqoru palmata (1-5 m depth) and A. cervicomis zones (5-15 m), so-called
because of the preponderance of these two coral species (Goreau, 1959; Kinzie, 1973 ;
Lang, 1974), were severely damaged by Hurricane Allen (Woodley et al., 198 1). Huston
(1985) reported 57, 42, and 27% cover by corals at 1, 10, and 20 m depths on the
forereefs at Discovery Bay in 1977. By 1986, we found only 2, 6, and 7% cover,
respectively (Table V; t test, P < 0.00
1). Thus, coral cover on the forereefs has declined
dr~atically
over the last 6 yr, by x75-95%.
The majority of the reduction was
undoubtedly caused by the hurricane (Woodley et&., 1981). However, many of the
surviving corals surveyed in 1986 were partiahy overgrown by dense growths of algae,
which have reduced coral cover even further. Moreover, recovery of the damaged coral
populations has likely been seriously impaired by the recent algal bloom, because of the
susceptibility of coral recruits to competition with algae (e.g., Bak & Engel, 1979;
Hughes, 1985).
CORAL
COVER,
1983-
80
50
%
g
0
;2
8
0
40
1986
m
JUL 83
m
JUN84
m
@
JAN85
JUN85
B
JAN86
30
20
6(
10
0
7m
10m
15m
20m
Fig. 6. Coral cover vs. time (mean f SE) at 7,10,15 and 20 m depths at Rio Bueno, from the month before
the die-off of D. ~~ti~~~~ to September 1986.
HERBIVORYONCORA~REEFS
53
At Rio Bueno, coral populations have been monitored continuously, so the effects
of the algal bloom can be more clearly distinguished from the earlier hurricane damage.
At 7 and 10 m, coral cover has been reduced from 27 to 11% and from 43 to 24x,
respectively, since 1983 (Wilcoxon-signed rank test, P < 0.01; Fig. 6). This sharp
decline reversed an earlier increasing trend in cover by corals that were recovering from
the hurricane, and is the lowest amount of cover observed at Rio Bueno for over a
decade (Table I in Hughes Br Jackson, 1985). Careful examination of photographic
sequences of the permanent plots shows widespread overgrowth of corals by algae (e.g.,
Fig. 3). Coral-mortality rates in shallow water have increased over the past 3 yr, while
rates of recruitment have declined sharply (Hughes, in prep.) compared with levels
measured before the algal bloom (Hughes, 1984, 1985; Hughes & Jackson, 1985).
Deeper sites at Rio Bueno so far have shown no significant change in coral abundance
since 1983 (Wilcoxon-signed rank test, P > 0.05), probably due in part to the general
decline in amounts of algae at greater depths (Tables IV, V). In addition, coral species
in deeper water tend to be larger and longer-lived, and are often less susceptible to
competition with algae (Hughes, in prep.).
DISCUSSION
Large-scale events, such as hurricanes, invasions, or extinctions of species, often have
enormous impact on the dynamics of a community (e.g., Elton, 1958; Connell, 1978;
Pearse & Hines, 1979; Woodley et al., 1981; Diamond, 1986). The population crash of
D. antzlarum has coincided with a substantial increase in abundance of algae and a
corresponding decline of corals, resulting in a significant alteration of the community
and trophic structure of many Jamaican reefs.
Populations of D. antillarum remain at 0 or low levels > 3 yr after the initial die-off
(Table I). Sustained or heavy recruitment by Diadema that might have provided a rapid
recovery has evidently not taken place. Recent larval recruitment, indicated by the
presence of small urchins, has apparently occurred successfully at only three of the 11
sites we examined closely (the three backreef sites), Whether the paucity of juveniles is
caused by a lack of settlement or by high early mortality is unknown. It is also possible,
given the high growth rate of~~adema (Randall et al., 1964; Levitan, in press), that some
juveniles recruited soon after the die-off and are now fully grown, and indistinguishable
from older individuals. Migration of surviving adults between neighboring reefs might
also have occurred, and could account for some or all of the small increase at Rio Bueno
since 1983. Surviving Diadema and new recruits are often highly aggregated in small
patches (e.g., around a single coral head), reducing algal biomass again to low levels
but only at a very local scale. It may be a long time before Diadema once more reaches
densities that are sufliciently high to reduce algal abundance over whole reefs.
There was no general increase in numbers of other echinoids following the mass
mo~a~ties of D. a~tjlfa~rn (Table II), suggesting that interspecific competition with
54
T.P. HUGHES ETAL.
large numbers of Diudemu was not a factor limiting their abundance. Other sea urchins
were free of symptoms during the die-off in 1983 (Bak et al., 1984; Hughes et al., 1985;
Lessios et al., 1984b), and it would seem likely that the subsequent 3 yr would have been
sufficient for some response to take place (e.g., Cubit et al., 1986). However, the species
examined here differ significantly in diet and distribution. Echinometra viridis is much
less mobile and more cryptic than Diudema (Sammarco, 1982a). Lytechinus and
especially Tnipneustes are most often found in seagrass beds, where Diadema is relatively
uncommon (Ogden & Lobel, 1978; Keller, 1983). Only a little is known about shortor long-term fluctuations in populations of these urchins (see Lessios et al., 1984b;
Cubit et al., 1986), and it seems likely that the modest changes observed are unrelated
to the decline of L). ~~tilia~rn. Densities of other less conspicuous herbivores (e.g.,
gastropods, polychaetes, crustaceans, etc.) may have increased, but if so, they obviously
are not yet at levels sufficient to halt or reverse the dramatic changes in algal communities that have occurred. The current paucity of Diadema is also unlikely to be fully
compensated for in the future by substantial increases in fish stocks, given the continued
overfishing in Jamaica by humans.
The impact of the loss of D. antiifarum from Jamaica may be especially large
compared with elsewhere in the Caribbean. Hurricane Allen in 1980 substantially
reduced the percent cover by stony corals on shallow or exposed forereef sites on the
north coast of Jamaica (Woodley et al., 1981). If the coral cover had been higher when
the urchins died, it would almost certainly have taken longer for the algae to reach their
present abundance, since algae cannot settle on live coral tissue. In addition, the coral
reefs near Discovery Bay are relentlessly overfished, so that herbivorous scarids and
acanthurids are small and relatively scarce compared with more pristine reefs elsewhere
(Woodley, 1979; Hay, 1984). In the past, algal abundance in Jamaica was low (Brawley
& Adey, 1977; Carpenter, 1981; Hughes & Jackson, 1985), despite overfishing, in part
because of the presence of large numbers of D. antillarum. Indeed, it is likely that the
urchin populations were large because of reduced predation and competition from fish
(Woodley, 1979; Hay, 1984; Hay & Taylor, 1985). Thus, the recent increase in algae
described here may be due in part to the prior reduction of many species of herbivorous
fish, as well as the more recent decline of D. an~il~a~rn.
The relative importance of different herbivores has been drastically altered in the past
on many Caribbean reefs by overfishing (Woodley, 1979; Hay, 1984), and again more
recently by the mass mortalities of Diudema (Carpenter, 1985, 1986). The effects of the
decline of D. antillarum on algal communities may vary greatly from place to place
depending on the abundance of remaining herbivores. In contrast to the results
presented here, the algal biomass on patch reefs in St. John, where herbivorous fish are
relatively common, reached a maximum 6 months after the urchin die-off, and has since
declined steadily (Levitan, in press). The peak algal biomass was an average of 304 g
dry weight * m - ‘, which fell by April 1986 to only 50 g * m - 2, substantially less than any
of the reefs examined in Jamaica (see Table IV). Furthermore, coral cover has remained
steady in St John over the past 3 yr (Levitan, in press). On a smaller scale, it is likely
HERBIVORY
ON CORAL REEFS
55
that some of the site-to-site variation in the taxonomic composition of Jamaican algal
assemblages in 1986 (Fig. 4) is caused by spatial differences in the relative abundance
of many herbivores, including the surviving D. antibwm (cf. Hay, 1984; Hay & Taylor,
1985; Carpenter, 1985, 1986).
The die-off provides a unique opportunity to compare the results of previous removal
experiments performed in Jamaica (on Crosby and Stills Reefs; Sammarco, 1980,
1982a,b) with the aftermath of the natural demise of Diadema. Qualitatively, the results
of Sammarco’s manipulations were very similar to patterns observed following the mass
mortalities. In both cases, amounts of macro-algae increased substantially following the
decline in numbers of D. u~tilla~m (see also Ogden et&., 1973b; Sammarco et al.,
1974; Carpenter, 1981, 1985, 1986; Hay & Taylor, 1985). However, qu~titatively, the
results are rather different. Specifically, the increase in algal biomass following the
die-off was four times greater, resulting in the virtual elimination of corals on patchreefs
(‘Table V). In marked contrast, over the course of Sammarco’s study, coral cover on the
experimental reef (Stills Patch Reef) actually increased significantly from 36 to 48 y0 in
the absence of Diadema (Sammarco, 1982a), although many juvenile corals were
smothered by the developing algal communities. Thus, evidence from the field experiment and natural experiment for the r61e of Diadema in the dynamics of Jamaican reefs
is not in total concordance.
The scale of the experimental removal and die-off is of course very different, in both
space and time, which may account for much of the difference between their respective
outcomes. Sammarco’s control and experimental reefs, Crosby and Stills Patch Reef,
respectivefy, have a combined area of z 1000 m2 (Sammarco, 1982a). For logistic
reasons, this is about the largest area on which densities of Diadema antillarum could
be monitored and controlled and the response of algal and coral communities could be
measured. The die-off, on the other hand, occurred over several million square
kilometers (Lessios et al., 1984b). Following the die-off, virtually all shallow reefs
experienced a more or less simultaneous increase in algal abundance (e.g., Table IV),
and the effects of remaining herbivores, especially fish, were not concentrated in any
one small area. In contrast, when relatively small plots (e.g., single patch reefs) were
experiment~Iy cleared of Diadems, the biomass of algae increased IocalIy and densities
of herbivorous fish rose substantially compared with controls as the m~ipulated sites
became more attractive (e.g., Ogden et al., 1973b; Hay & Taylor, 1985; P. W.
Sammarco, pers. comm.). Presumably, ifthe numbers of fish on experimental reefs had
remained at ambient (control) levels, the algal response to experimental removals of
Diudema would have been even larger. In addition, a large-scale increase in algae would
presumably result in the increased availability of algal propagules, which could also
account for the much greater abundance of algae on Crosby and Stills Reefs today
compared with the maximum observed by Sammarco (1982a,b).
The significant differences between Sammarco’s experimental results and the die-off
may also be due to their respective durations. Sammarco’s manipulation to reduce
numbers of Diudema a~~~Z~a~rnlasted for 18 months, which is considerably longer than
T.P.HUGHES ETAL.
56
most field experiments
(Schoener,
by the die-off has continued
1983). The virtual elimination
of D. antillarum caused
twice as long, so far. The time course of the algal bloom
after the die-off (Fig. 5) suggests that the amount of algae observed by Sammarco was
probably not at equilibrium after 18 months. Even after more than 3 yr since the mass
mortalities, algae continue to increase (Fig. 5), while corals in shallow water decline
(Fig. 6). If D. antillarum and fish remain scarce for much longer, it is likely that the recent
changes in community structure will continue, resulting in further replacement of corals
by algae in shallow water. Additional studies of the consequences
of the urchin mass
mortalities should provide valuable insights concerning the role of herbivory on tropical
reef communities.
ACKNOWLEDGEMENTS
We thank C. Ala Imo, G. Bruno, R.C. Carpenter,
M. Carr, J.H. Connell, C.
D’Antonio, A. W. Ebeling, J. B. C. Jackson, R. H. Karlson, P. Raimondi, S. Schroeter,
E. Schultz, and R.S. Steneck for their help and encouragement.
Don Levitan and Paul
Sammarco generously provided unpublished
data. Mark Hay and an anonymous
reviewer gave helpful and insightful comments. Major funding for this research was
provided by a grant from the National Geographic Society (Grant 3382-86) awarded
to T. P. Hughes. Additional support was provided by NSF grants to J. H. Connell (OCE
84-08610 and 86-08829) and J.B.C. Jackson (OCE 84-15712), and by grants to T. P.
Hughes from the Whitehall Foundation
and the American Philosophical
Society.
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