Herbivory on coral reefs: community structure following mass

J. Exp. niiar. B&l. Ecol., 1987, Vol. 113, pp. 39-59 Elsevier

39

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). Con- sequently, 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

HERBIVORY ON CORAL REEFS 41

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~~~~rn in 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.


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 o C for 24-48 h, and weighed again. Finally, the algae were decalcified with a 5% acid solution, dried, and weighed a third time.

HERBIVORY ON CORAL RE FS 43

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)

Before die-off+ After die-off

September 1983 September 1986

Rackreefs Inner Reef Crest lm 3.9 f 7.4 (116) 0.35 + 0.55 (20) Crosby Patch Reef 2m 71.0 + 19.5 (8) 0.80 * 1.01 (20) Stills Patch Reef 2m 33.5 f 16.7 (8) 0.35 * 0.75 (20) Forereefs Dancing Lady 8m 10.5 5 7.2 (20) 0.05 f 0.22 (20) 0

15m 4.7 + 2.4 (20) 0 (20) 0 Mooring 1 3m 8.1 f 0.7(33) 0

10.5 m 12.2 f 4.3 (17) 0 Pear Tree Bottom 10 m 8.9 f 5.5 (21) 0 (20) 0 lpio Buena

7m 11.7 + 7.6(16) 0.15 f 0.25 (16) 0.15 & 0.37 (20) 10m 3.5 * 7.3 (66) 0.08 f 0.10 (66) 0.45 & 0.71 (40) 20 m 0.7 + 0.8 (6) 0 (20) 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


TABLE III

Sum

mar

y of

alg

al a

bund

ance

. A

ll bi

omas

s es

timat

es

are

per

m*.

Sta

tistic

al

test

s be

twee

n al

l se

ts

of o

bser

vatio

ns

are

not

poss

ible

be

caus

e of

dif

fere

nt

met

hodo

io~e

s.

For

all s

ites

com

bine

d,

ther

e w

as a

sig

nifi

cant

inc

reas

e in

alg

ae f

ollo

win

g th

e di

e-of

f (P

= 0

.002

, sig

n te

st).

Sou

rces

: (1

) B

raw

ley

& A

dey

(197

7);

(2)

Sam

mar

co

(198

2a);

(3)

Car

pent

er

(198

1);

(4)

pres

ent

stud

y,

mac

roal

gae

defi

ned

as t

hose

sp

ecie

s la

rge

enou

gh

to b

e se

en

in p

hoto

grap

hs

of l

ong-

term

qu

adra

ts;

(5)

tran

sect

da

ta

in H

ughe

s &

Jac

kson

(1

985)

, in

clud

es

both

m

acro

alga

e an

d sm

alle

r tu

rfs.

Site

D

epth

(m)

Bef

ore

die-

off*

(d

ate)

A

Rer

die

-off

(Se

ptem

ber

1986

)

Bac

kree

f In

ner

Ree

f C

rest

C

rosb

y Pa

tch

Ree

f St

ills

Patc

h R

eef

Fore

reef

M

oori

ng 1

Moo

ring

1

Dan

cing

L

ady

Rio

Bue

no

lm

2m

2m

2-3

m

10m

20

m

7m

10m

20 m

2.38

kg

wet

m -

z (1

974)

’ 6-

29 g

dec

al.

m -

’ ( 1

973-

75)2

5.

5 g

deca

l. m

-’

(197

3)’

22%

cov

er

by n

oncr

usto

se

alga

e (1

978)

3 40

% c

over

by

non

crus

tose

al

gae

(197

8)3

34g

wet

rn-

’ (1

974)

’

3% c

over

by

mac

roal

gae

(198

3)’

< 1

% c

over

by

non

crus

tose

al

gae

( 197

7)5

< 1

% c

over

by

mac

roal

gae

( 198

3)4

~2%

co

ver

by n

oncr

usto

se

alga

e ( 1

977)

5 <

2%

cov

er

by m

acro

alga

e ( 1

983)

4

4.55

kg

wet

m ._

2 (T

able

IV

) -I

196

g de

cal.

m-*

(T

able

IV

) Y

228

g de

cal.

ma2

(T

able

IV

) z

95%

cov

er

by n

oncr

usto

se

alga

e (T

able

V)

3

94%

cov

er

by n

oncr

usto

se

alga

e (T

able

V)

G

1.79

kg

wet

m -

’ (T

able

IV

)

9 1%

cov

er

by n

oncr

usto

se

alga

e (T

able

V)

87%

cov

er

by m

acro

alga

e (F

ig. 5

) 72

% c

over

by

non

crus

tose

al

gae

(Tab

le V

) 13

% c

over

by

mac

roal

gae

(Fig

. 5)

8 1%

cove

r by

non

crus

tose

al

gae

(Tab

le V

) 15

% c

over

by

mac

roal

gae

(Fig

. 5)

_


viridis, actually declined significantly on both Crosby and Stills Reefs (t test, P < 0.05 and P < 0.001, respectively). Lytechinus williamsi increased 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,



BACKREEF

P E

FOREREEF

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

Wet weight 4554 + 802 2352 + 733 1212 + 215 Dry weight 1730 * 388 435 f 89 313 + 54 Decalcified dry weight 422 & 82 196 f 45 228 & 43 --...

Forereef

2m 10m 20m

Wet weight 439 I: 119 3253 + 1020 1791 + 391 Dry weight IlO* 1436 f 612 846 k 232 Decalcified dry weight 39rt 11 303 + 106 186 + 51 _-_- -

Rio Bueno ~--

7m IO m 20 m ~_ _.-...

Wet weight 4124 -t_ 1402 543 k 448 500 + 217 Dry weight 2280 F 847 315 & 288 230 + 116 Decalcified dry weight 496 + 208 84 k 75 41 + 26


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.

Afgae Hard corals Soft corals Sponge Sand

~.-

Inner Reef Crest

87.3 + 9.2

0.1 * 0.2 0

0 13.6 I 11.0

Backreef

Crosby Patch Reef

94.2 f 5.0 2.6 f 2.1

3.2 t 4.2 0.2 * 0.4

0

Stills Patch Reef I~

94.6 & 2.0 2.3 F 1.5 3.0 * 1.7

0.4 & 0.9 0

Forereef

2m 10m 20 m

Algae 95.2 rt 4.2 93.9 2 4.5 86.2 + 8.2

Hard corals 2.0 $ 1.8 5.8 & 2.1 7.0 + 4.2

Soft corals 2.6 f 2.3 0.3 + 0.3 0.4 & 0.4

Sponge 0 0 1.2 & 1.6

Sand 0.1 * 0.3 0 5.2 t 6.4

Rio Bueno

7m 10m 20 m - _. .-.___I_

Algae 90.6 k 4.1 72.4 k 2.8 80.9 + 9.3

Hard corals 8.2 i: 3.9 23.9 & 3.4 13.1 i 7.5

Soft corals 1.2 + 2.2 3.4 * 2.0 1.5 rt 2.3

Sponge 0 0.3 + 0.7 4.5 i 2.9

Sand 0 0 0


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 COVER, 1983 - 1986

: 80 (9

;1

k 60

5 40

B

z 20

0 7m IOm

W JUL 83

tg JAN84

f-1 JUN 84

CII JAN85

I-:] JUN 85 [:-I JAN 8 6

i_? SEP 86

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).

52 T. P. HUGHES ET&.

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- 1986

m JUL 83

80 m JUN84

50 m JAN85

% @ JUN85

g 40 B JAN86

0

;2 30

8 0 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 short- or 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


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~rn lasted for 18 months, which is considerably longer than

56 T.P.HUGHES ETAL.

most field experiments (Schoener, 1983). The virtual elimination of D. antillarum caused

by the die-off has continued 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.

REFERENCES

ADEY, W.H., P.J. ADEY, R. BURKE & L. KAUFMAN, 1977. The Holocene reef systems of eastern Martinique, French West Indies. Atoll Rex Bull., No. 218.

ADEY, W.H. & R.S. STENECK, 1985. Highly productive eastern Caribbean Reefs: synergistic effects of biological, chemical, physical and geological factors. In, The ecology of coral reefs, NOAA Symp. Ser. Undersea Res., Vol. 3, edited by M.L. Reaka, NOAA Undersea Research Program, Rockville, pp. 163-187.

BAK, R. P. M., M. J. E. CARPAY & E. D. DE RUYTER VAN STEVENINCK, 1984. Densities of the sea urchin Diudema antillurum before and after mass mortalities on the coral reefs of Curacao. Mar. Ecol. Prog. Ser., Vol. 17, pp. 105-10s.

BAK, R. P.M. & M. S. ENGEL, 1979. Distribution, abundance and survival of juvenile hermatypic corals (scleractinia) and the importance of life history strategies in the parent coral community. Mar. Biol., Vol. 54, pp. 341-352.

BIRKELAND, C., 1977. The importance of rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. In, Proceedings of the 3rd International Coral Reef Symposium Miami, pp. 15-21.

BOROWITZKA, M., 1981. Algae and grazing in coral reef ecosystems. Endeavour, N.S., Vol. 5, pp. 99-106. BRAWLEY, S. H., ADEY, W. H., 1977. Territorial behavior ofthree spot damselfish (EupomacentruspluniJ?ons)

increases reef biomass and productivity. Environ. Biol. Fish., Vol. 2, pp. 45-51. CARPENTER, R.C., 1981. Grazing by Diadema antillurum Philippi and its effects on the benthic algal

community. J. Mar. Res., Vol. 39, pp. 749-765. CARPENTER, R.C., 1985. Sea urchin mass-mortality: effects on reef algal abundance, species composition,


and metabolism and other coral reef herbivores. In, Proceedings of the 5th International Reef Congress, Vol. 4, Antenne Museum-Ephe, Moorea, French Polynesia, pp. 53-60.

CARPENTER, R.C., 1986. Partitioning herbivory and its effects on coral reef algal communities. Ecol.

Monogr., Vol. 56, pp. 345-363.

CONNELL, J.H., 1978. Diversity in tropical rain forests and coral reefs. Science, Vol. 199, pp. 1302-1310. CONNOK, J. L. & W. H. ADEY, 1977. The benthic algal composition, standing crop, and productivity of a

Caribbean algal ridge. Atoll Res. Bull., No. 211, pp. l-40. CUBIT, J. D., D. M. WINDSOR, R. C. THOMPSON & J. M. BURGET~, 1986. Water-level fluctuations, emersion

regimes, and variations of echinoid populations on a Caribbean reef flat. Estuarine Coastal Shelf Sci., Vol. 22, pp. 719-737.

DE RUYTER VAN STEVENINCK, E.D. & A.M. BREEMAN, 1981. Biomass and relative coverage of benthic algae in the fore-reef of Curacao (Netherlands Antilles) in relation to production. Mar. Ecol. Prog. Ser., Vol. 6, pp. 257-265.

DIAMOND, J., 1986. Overview: laboratory experiments, held experiments, and natural experiments. In, Community ecology, edited by J. Diamond & T. J. Case, Harper and Row, New York, pp. 3-22.

DOTY, M. S., 1971. Antecedent event influence on benthic marine algal standing crops in Hawaii. J. Exp.

Mar. Biol. Ecol., Vol. 6, pp. 161-166. ELTON, C. S., 1958. The ecology of invasions by animals and plants. Methuen, London. 181 pp. GOREAIJ, T. F., 1959. The ecology of Jamaican coral reefs. I. Species composition and zonation. Ecoloa,

Vol. 40, pp. 67-89. EIATCHI:R, B. G. & D. W. RIMMER, 1985. The role of grazing in controlling benthic community structure

on a high latitude coral reef: measurements of grazing intensity. In, Proceedings of the 5th International Coral Reef Congress, Vol. 6, Antenne Museum-Ephe, Moorea, French Polynesia, pp. 229-236.

E~AY, M. E., 1981. Herbivory, algal distribution, and the maintenance of between-habitat diversity on a

‘tropical fringing reef. Am. Nat., Vol. 118, pp. 520-540. EIAY, M. E., 1984. Patterns of fish and urchin grazing on Caribbean coral reefs: are previous results typical?

Ecolggy, Vol. 65, pp. 446-454.

FIAY, M. E., 1985. Spatial patterns of herbivore impact and their importance in maintaining algal species richness. In, Proceedings of the 5th International Coral Reef Congress, Vol. 4, Antenne Museum-Ephe, Moorea, French Polynesia, pp. 29-34.

HAY. M. E., T. COLBURN & D. DOWNING, 1983. Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia (Berlin), Vol. 58, pp. 299-308.

HAY, M. E. & P.R. TAYLOR, 1985. Competition between herbivorous fishes and urchins on Caribbean reefs.

Oecologia (Berlin), Vol. 65, pp. 591-598.

HUGHES, T. P., 1984. Population dynamics based on individual size rather than age: a general model with a reef coral example. Am. Nat., Vol. 123, pp. 778-795.

EIUGHES, T. P., 1985. Life histories and population dynamics of early successional corals. In, Proceedings of the 5th International Coral Reef Congress, Vol. 4, Antenne Museum-Ephe, Moorea, French Polynesia, pp. 104-106.

HUGHES, T. P. & J. B. C. JACKSON, 1985. Population dynamics and life histories of foliaceous corals. Ecol. Monogr., Vol. 55, pp. 141-166.

EIUGHES, 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.

EIUNTE, W., I. COTE & T. TOMASCIK, 1986. On the dynamics of the mass mortality of Diadema antillamm in Barbados. Coral Reefs, Vol. 4, pp. 135-139.

EIUNTEK, I.G., 1977. Sediment production by Diadema antillarum on a Barbados fringing reef. In,

Proceedings of the 3rd International Coral Reef Symposium, Vol. 2, pp. 105-l 10. EIUSTON, M., 1985. Patterns of species diversity in relation to depth at Discovery Bay, Jamaica. Bull. Mar.

Sci., Vol. 37, pp. 928-935.

KARLSON, R.H., 1983. Disturbance and monopolization of a spatial resource by Zoanthus sociatus (Coelenterata, Anthozoa). Bull. Mar. Sci., Vol. 33, pp. 118-131.

KELLER, B.D., 1983. Coexistence of sea urchins in sea-grass meadows: an experimental analysis of competition and predation. Ecology, Vol. 64, pp. 1581-1598.

KINZIE, R.A., III, 1973. The zonation of West Indian gorgonians. Bull. Mar. Sci., Vol. 23, pp. 93-155.


KNOWLTON, N., J.C. LANG, M.C. ROONEY & P. CLIFFORD, 1981. Evidence for delayed mortality in hurricane-damaged Jamaican staghorn corals. Nature (London) Vol. 294, pp. 251-252.

LANG, J., 1974. Biological zonation at the base of a reef. Am. Sci., Vol. 62, pp. 272-281. LESSIOS, H. A., D. R. ROBERTSON & J. D. CUBIT, 1984a. Spread of Diudema mass mortality through the

Caribbean. Science, Vol. 226, pp. 335-337. ~_assros, H.A., J.D. CUBIT, D.R. ROBERTSON, M.J. SHUI.MAN, M.R. PARKER, S.D. GARRITY & SC.

LEVINGS, 1984b. Mass mortality of Diudema antillarum on the Caribbean coast of Panama. Coral Reefs, Vol. 3, pp. 173-182.

LEVITAN, D., Effect of reduced population density on body size in the sea urchin Diadema antillarum (Philippi): evidence of release from food limitation, in press.

LEWIS, J. B., 1964. Feeding and digestion in the tropical sea urchin Diadema antilfarum Philippi. can. J. Zool., Vol. 42, pp. 549-551.

L~wrs, S. M., 1986. The role of herbivorous fishes in the organization of a Caribbean reef community. EC& Mono~.~ Vol. 56, pp. 183-200.

LIDDELL, W.D. & S. L. OHLHORST, 1986. Changes in benthic community composition following the mass mortality of Diadema at Jamaica. J. Exp. Mar. Biol. Ecol., Vol. 95, pp. 271-278.

LOBEL, P., 1980. Herbivory by damsellishes and their role in coral reef community structure. In, Biology of damselfishes, edited by A. R. Emery % R. E. Thresher, RUN. Mar. Sci., Vol. 30, pp. 273-289.

OGDEN, 1977. Carbonate-sediment production by parrottish and sea urchins on Caribbean reefs. In. Reefs and related carbonates-ecology and sedimentology, edited by G.H. Frost, M.P. Weis & J. B. Saunders. Am. Assoc. Petrol. Geol. Stud. Geol., Vol. 4, pp. 281-288.

OGDEN, J.C., D.P. ABBOTT & LA. ABBOTT, eds., 1973a. Studies on the activity and food of the echinoid Diudema antillarum Philippi on a West-Indian Patch Reef. West Indies Lab. Spec. Publ., Vol. 2, 96 pp.

OGDEN, J. C., R.A. BROWN & N. SALESKY, 1973b. Grazing by the Echinoid Diadema antillarum Philippi: formation of halos around west Indian Patch reefs. Science, Vol. 182, pp, 715-717.

OGDEN, J. C. & P.S. LOBEL, 1978. The role of herbivorous lishes and urchins in coral reef communities. Environ. Biol. Fish., Vol. 3, pp. 49-63.

PEARSE, J. S. & A. H. HINES, 1979. Expansion of a central California kelp forest following the mass mortality of sea urchins. Mar. Bioi., Vol. 51, pp. 83-91.

POTTS, D. Cr., 1977. Suppression of coral populations by filamentous algae within damselfish territories. J. Exp. Mar. Biol. Ecol., Vol. 28, pp. 207-216.

RANDALL, J. E., A. E. SCHROEDER & W. A. STARCK, II, 1964. Notes on the biology of the echinoid Diadema antillarum. Caribb. J. Sci., Vol. 4, pp. 421-433.

SAMMARCO, P. W., 1977. Grazing by Diudema antillurum on a shallow-water coral reef community. Ph.D. dissertation. State University of New York at Stony Brook, 371 pp.

SAMMARCO, P. W., 1980. Diudema 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. f&p. Mar. Biol. Ecol., Vol. 61, pp. 31-55.

SAMMARCO, P. W., 1982b. Effects of grazing by Diadema anfi~~o~m Philippi (Echinodermata : Echinoidea) on algal diversity and community structure. J. Exp. Mar. Bioi. Ecu!., Vol. 65, pp. 83-105.

SAMMARCO, P. W., 1983. Effects of fish grazing and damsel&h ter~to~ality on coral reef algae. I. Algal community structure. Mar. Ecol. Prog. Ser., Vol. 13, pp. l-14.

SAMMARCO, P. W., J. S. LEVINTON & J.C. OGDEN, 1974. Grazing and control of coral reef community structure by Diadema anlillarum Philippi (Echinodermata : Echinoidea): a preliminary study. J. 1Mar. I&., Vol. 32, pp. 47-53.

SCHOENER, T. W., 1983. Field experiments on inter-specific competition. Am. Nut., Vol. 122, pp. 240-285. SCOFFIN, T.P., C.W. STEARN, D. BOUNCHER, P. FRYDL, CM. HAWKINS, I.G. HUNTER SC J.K.

MACGEACHY, 1980. Calcium carbonate budget of a fringing reef on the west coast of Barbados. II. Erosion, sediments and internal structure. Bull. Mar. Sci., Vol. 30, pp. 475-508.

VINE, P. J., 1974. Effects of algal grazing and aggressive behavior offishes Pomacentrus lividus and Acanthurus sohal on coral reef ecology. Mar. Biol., Vol. 24, pp. 131-136.

VOOREN, C. M., 1981. Photosynthetic rates of benthic algae from the deep coral reef of Curacao. Aq. Bat., Vol. 10, pp. 143-154.

WANDERS, J. B. W., 1976. The role of benthic algae in the shallow reef of Curacao. (Netherlands Antilles). II. Primary productivity ofthe S~~~surn beds on the north-east coast submarine plateau. Aq. Bor., Vol. 2, pp. 327-335.


WANDERS, J. B. W., 1976. The role of benthic algae in the shallow reef of Curacao (Netherlands Antilles). III. The significance of grazing. Aq. Bat., Vol. 3, pp. 357-390.

WILLIAMS, A. H., 1979. Interference behavior and ecology of threespot damselfish (Eupomacentrus

planifrons). Oecologia (Berlin), Vol. 38, pp. 223-230. WOODI.EY, J. D., 1979. The effects of trap-fishing on reef communities in Jamaica. In, Proceedings of 13th

Meeting of the Association of Island Marine Laboratories of the Caribbean, Abstracts, University of Puerto Rico. Mayaguez, Puerto Rico, p. 27.

WOODI.EY, J.D., E.A. CHORNESKY, P.A. CLIFFORD, J.B.C. JACKSON, L. S. KAUFMAN, 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, & E.M. SIDES, 1981. Hurricane Allen’s impact on Jamaican coral reefs. Science, Vol. 214, 749-755.

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Herbivory on coral reefs: community structure following mass