Bleaching and hurricane disturbances to populations of coral recruits in Belize
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MARINE ECOLOGY PROGRESS SERIES
h b l i s h e d December 14
Mar Ecol Prog Ser
Bleaching and hurricane disturbances to
populations of coral recruits in Belize
Peter J. Mumby*
Centre for Tropical Coastal Management Studies, Department of Marine Sciences and Coastal Management,
Ridley Building. University of Newcastle, Newcastle upon Tyne NE1 7RU. United Kingdom
ABSTRACT: In 1998, coral populations in Belize were disturbed sirnultaneously by a severe coral
bleaching event and Hurricane Mitch. The impact of these disturbances was assessed for naturally
occurring populations of coral recruits (2 to 20 mm diameter), at a depth of 8 to 10 m on the forereef of
Glovers Atoll. Bleaching took place at aii 4 study sites but the hurricane only affected 2 sites, enabling
the effects of bleaching to be compared to those arising from bleaching plus hurncane damage. Pre-
disturbance recruit density, size-frequency distribution, and cornmunity structure were similar be-
tween sites (at kiiometre scales). The bleaching event lasted ca 3.5 mo. From 70 to 90% of adult
colonies bleached and at least 25% of recruits exhibited signs of bleaching. A month after adult colonies
had regained usual colouration, only 1 % of recruits showed even partial bleaching. Surprisingly, coral
bleaching alone had no measurable effect on either recruit density or community structure. The com-
bination of bleaching and hurricane disturbance reduced total recruit densities to 20% of pre-&stur-
bance levels. Effects of bleaching/hurricane disturbance on community structure were spatially patchy,
and I suggest that such patchiness may arise from variable Cover of protective rnicrohabitat and/or dif-
ferent storm conditions mediated by proximity to reef cuts (breaks in the reef crest).
KEY WORDS: Coral recruitment . Bleaching . Hurricane Mitch . Mortality . Cornmunity structure
INTRODUCTION severest hurricane event at Glovers Atoll since Hurri-
canes Greta in 1978 and Hattie in 1961 (see Stoddart
From September to December 1998, coral popula- 1963, Stoddart et al. 1982).
tions in Belize expenenced two of the most severe dis- Here, I document the effects of bleaching and hurri-
turbances of recent decades: massive coral bleaching cane events on coral recruits occurnng naturally on the
and Hurncane Mitch. Coral bleaching refers to the pal- forereefs at Glovers Atoll. Recruits are defined as juve-
ing of coral tissue brought about by a loss of coral's nile corals at the size of first sighting in the adult habi-
zooxanthellate symbionts and/or a breakdown of zoo- tat (Caley et al. 1996),which encompasses diameters of
xanthellate pigments (Glynn 1993, Brown 1997). The 2 to 20 mm in this study (see also Hughes 1985). Corals
1997/8 bleaching event in Belize was Part of the most on the seaward side of the atoll expenenced both
widespread bleaching event ever recorded and was bleaching and hurricane events, whereas populations
probably attributable to anomalies in maxirnum sea- on the leeward side were sheltered and expenenced
water temperatures and solar irradiance (International bleaching but no apparent mechanical damage from
Society for Reef Studies 1998). In late October (during the hurricane. By surveying recruits shortly before and
the bleaching), the eye of Hurricane Mitch passed after these disturbance events, and on opposite sides of
approximately 200 km south-east of Glovers Reef. Hur- the atoll, I compare the impacts of bleaching with the
ricane Mitch was a category 5 storm and was the combination of bleaching and Hurncane Mitch. As far
as I am aware, this is the first study to examine the
effects of bleaching and hurncanes on juvenile Carib-
bean corals. Specificaliy, I ask the following questions
Q Inter-Research 1999
Resale of full artide not permitted28 Mar Ecol Prog Ser 190: 27-35, 1999
with respect to an offshore atoll in Belize: (1) Does a ardly. Care was taken to inspect cryptic habitats (e.g.
severe bleaching event (as defined by the degree of between Montastraea knobs) in which recruits were
bleaching on adult colonies) lead to net mortality of often found. Each site was located near the drop-off
recruits? (2) What is the net post-recruitment mortality and was dominated by Montastraea annularis and M.
rate ansing from the combination of bleaching and faveolata. Sites measured approximately 60 by 30 m
Hurncane Mitch? (3) How do bleaching and 'bleaching and depth ranged between 8 and 10 m. The maxi-
plus hurricane' events affect the community structure mum diameter of each recruit was measured using a
of recruits? clear rule and species identification was made when
Synergistic effects between bleaching and hurricane possible. Recruits ansing from asexual fragmentation
disturbance tvere not exarnined because no site expe- of branching colonies (Hughes 1985) were ignored as
nenced hurncane damage but no bleaching. were (rare) cases where larger juveniles (>20 mm dia-
meter) of massive species had fragmented into recruit-
sized daughter colonies. The diameter of the smallest
METHODS observable recruit was 2 mm but species designation
was not possible, and therefore data are reported here
Surveys were conducted at 4 sites on Glovers Atoll by genus. Replication differed during pre-disturbance
(Fig. 1). Sites on the seaward forereef (East 1 [El] and sunreys: 2 transects were surveyed at W2, 6 at E2, ? at
East 2 [E2]) experienced bleaching and hurricane da- W1, and 10 at El. Sample size for post-disturbance
mage whereas leeward sites (West 1 [Wl] and West 2 surveys (14 transects, except W2 which had 13) was
[W2]) only experienced bleaching. Sampling for re- determined for a 90% power of detecting a 2-sample
cruits was conducted in late July 1998 and January differente in density of 6 recruits (sample standard de-
1999, which equates to ca 5 wk before the bleaching viation) based on the pooled standard deviation of
and 4 wk after the end of bleaching, and 3 mo before pre-disturbance data. Measurements of adult coral
the hurricane and 2 mo after the hurncane. In situ Cover where made using 18 replicate 1 m2 quadrats
bleaching observations were made in early October. per site.
Recruitment was measured by the same diver visu- Overall differences in recruit density were tested
ally inspecting replicate 10 by 0.5 m belt transects ori- using a 2-factor unbalanced general linear model
entated parallel to the reef crest and located haphaz- ANOVA (Minitab 1997) with sites and tirnes as fixed
MEXICO
- ..
--- ...
-:- ..-
- 17"N
GUATEMALA
- IOD km
- -
- --
--8g0W
-..:
Prevailing direction of
Hurricane Mitch
Fig. 1. Distribution of sampling sites at Glovers Atoll (= Glovers Reef) showing the location of reef cuts (breaks in the reef crest)
and the path of Hurncane MitchMumby: Bleaching and hiirricane damage to coral recruits 29
factors. Multiple cornparisons were defined a priori tially bleached d u n n g October (n = 130) but only
and examined using Bonferroni tests. The size-fre- 5 recruits (of 374 censused) were partially bleached by
quency distribution of recruits was examined using January 1999 and none were fully bleached (see
4 classes: 2-5, 6-1.0, 11-15 and 16-20 mm. To investi- McField 1999 for discussions of full and partial bleach-
gate the effects of disturbance on the structure of ing).
recruit cornrnunities at each site, comrnunity distance With 7 m seas for several days, Hurricane Mitch
was measured using the Bray-Curt1.s similarity co- caused extensive damage to shallow reefs removing ca
efficient and represented using non-metric multidi- 90% of living Acropora palmata at some sites. Direct
mensional scaling (MDS). The Bray-Curtis similarity darnage to adult corals at Sites E1 and E2 (8 to 10 rn)
coefficient has a number of desirable properties for will be reported elsewhere but ca 85% of large Mon-
measuring community similarities, such as ignoring tastraea annularis colonies showed recent partial mor-
joint absences of species (Mumby et al. 1996),and. is a tality.
robust measure of ecological distance (Faith et al.
1987). MDS is a widely used method of presenting
multivariate differences in community structure be- Spatial patterns of recruitment
tween samples in 2 dimensions (Clarke 1993). Data
were averaged per site without transforrnation. Differ- Pre-disturbance densities of recruits were similar
ences in community structure were examined using among sites (Fig. 2): ca 10 recruits per 5 rn2 transect.
similarity percentage (SIMPER) analysis of the contri- Unbalanced ANOVA gave highly significant main
bution made by each genus to mean inter-site dissimi- effects of site and time, and site-time interactions
larity (See Clarke 1993). (Table 1).Bonferroni multiple cornparisons (not shown)
revealed that recruit density did not vary significantly
between sites before the disturbances. Overall re-
RESULTS cruitment levels after the bleaching event (at Sites W1
and W2) were not significantly different to pre-
General impacts of coral bleaching a n d Hurricane bleaching levels. Significant ANOVA effects were
Mitch at Glovers Atoll attributable to the reduction of recruits at eastern sites
following the combination of bleaching and Hurricane
The 1998 coral bleaching event began in early Sep- Mitch ( p < 0.001) The reduction of recruitment den-
tember following a rnonth of calm weather and in- sity at eastern sites was remarkably consistent: 80 and
creasing water temperature (to 29 to 32"C, depending 81:,0 of pre-disturbance levels at Sites E1 and E2
on the site, T. J . Bright pers. comm.). Most adult corals respectively. Conversely, recruitment density showed
showed recovery of colouration by late December 1998 only a 1"/o decrease at Site W1 and a 3 % increase at
(i.e. 3 to 4 mo later). Early signs of bleaching-induced Site W2.
partial mortality (large patches of
recently dead tissue overgrown
with filamentous algae) on adult
IWr - --
Bleach ing only Bleaching & Hurricane
16 -
corals at Sites \V1 a n d W2 sug-
gested that Agaricia spp. experi-
1.1 -
enced the greatest partial mortal-
ity (ca 20%, Mumby unpubl.
-
data) . Acropora cervicornis is not
common ( 1 2 % total benthic CO-
ver), and ca 20% of total colony
area has died recently. Recent 2
rnortality on adult Montastraea
spp. and Porites spp. was ca 10
a n d 5 % respectively (Mumby
unpubl. data). During the bleach-
ing event, 70 to 90% of adult
colonies a w ~ e a r e dto be either
1 L
fully or partially bleached at all West I West 2 East I Easi 2
sites (Mumby unpubl' data' M' D' Fig. 2.Overall patterns in recruitment density for aii genera. Open bars: pre-distur-
McField Pers. *pproxi- bance (July 1998) data, solid bars: post-disturbance (January 1999) data. Error bars:
mately 25 % of recruits were par- standard errorl o n a plepuels :sieq i o i i g . e p p (6661A~enuey)
a~ueqrnlsrp-lsod:sleq pqos ' e p p (8661 hpy) asueqinls!p-ald :sleq uado .aseqd 6uqdures qsea Buunp ' a l ~ sqJea Je slrnl~alne loj suognqulsrp K>uanbaij-az~s.E '61d
(uiui) ssep laiauie!a
-
OZ 91 S I - II 01 -9 S-2
(uiui) ssep Ialauie!aMumby: Bleaching and hurncane damage to coral recruits
Table 1 Unbalanced general Linear model ANOVA comparing recruit density change community structure. HOW-
between sites, sampiing times, and their interaction ever, the bleaching/hurricane impacts
were site-specific resulting in different
Source df Sequential SS Adjusted SS Adjusted MS F p communities at Sites E1 and E2 (Fig. 4,
Table 2).
Site 3 675 263 87 5.67 0.002
Time
Table 2 shows how the combination
1 623 316 316 20.4232 Mar Ecol Prog Ser 190: 27-35, 1999
Table 2 . Differences in community structure of eastern sites, E1 and E2, before and after settlement mortality, (2) popu-
the combined bleachng and hurricane disturbances. Contnb.: absolute contnbution of lations are not strongly recruit-
-1
each genus to the overaii dissirnilarity between cornmunities E1 and E2 in a given ment limited but settlement
sampling period and Sums to total dissimiiarity between sites
space and post-settlement mor-
tality are similar between sites,
Genus Pre-disturbance communities Post-disturbance cornrnunities
and (3) populations are not
Mean colony density Contnb. Mean colony density Contrib.
(~m-~) (5m-') recruitment limited but post-
E1 E2 E1 E2 settlement mortality is highly
;
density-dependent. These ex-
Agaricia planations cannot b e elimi-
Pontes
Stephanocoenia nated at present and further
Siderastrea studies are needed to examine
i'vlontastraea 0.07 spatio-temporal dynamics of
Leptoseris 0.50 larval supply, settlement space,
Scolymia 0.07
and post-settlement mortality
Madracis 0.00
Mycetophyilia 0.07 2 at different sampling grains
Colpophyllia 0.14 4 (sample unit sizes) as well as
spatial distances (Caley et al.
1996, Mumby 1999).
The density, size-frequency distribution, and com- It is tempting to suggest that the dorninance of
munity structure of recruits were found to be highly recruits in the 6 to 10 mm size category may represent
consistent between sites before the bleaching and a large-scale early summer recruitment event. How-
hurricane disturbances began. This was surprising ever, densities of the sinaiiest recruits in this size class
considering that sites were drawn from opposite sides (2 and 3 mm diameter) were probably underestimated
of Glovers Atoil and the spatio-temporal Patterns of during visual sampling even though cryptic habitats
recruitment usually show great vanation. The scale of were scrutinised carefully. The 2 to 5 mm class is prob-
the study may provide some insight into the apparent ably a better record of 4 to 5 rnrn recruits. The propor-
uniforrnity of community characteristics. Edmunds et tion of 2 to 3 mrn corals ranged from 0 to 4 % of total
al. (1998) described an appropriate sampling strategy recruit abundance, so undersampling had Little impact
for juvenile corals (0.4 to 5.0 cm diameter) to consist of on the conclusions reached by this study, although
seventeen 0.25 m2 quadrats placed along 4 transects very recent (Mumby: Bleaching and hurricane damage to coral recruits 33
the population dynamics of juvenile corals. I suggest at have been compensated by recruitment and growth.
least 4 possible explanations for the apparent absence Future studies are needed to examine population
of bleaching-induced mortality. Experimental tests a r e dynamics at various temporal scales and with manipu-
necessary to discriminate among them. lations in recruit density. Empirical studies are also
needed on the effects of bleaching on juvenile growth
rate, but, as I point out next, local conditions may miti-
(1)Did juveniles experience a severe bleaching event? gate the influence of bleaching on growth.
Few studies of in situ bleaching (if any) have specifi-
cally examined whether juvenile corals expenence (3) Did heterotrophic feeding on sediments mitigate
similar bleaching responses to those exhibited by adult reduced autotrophic nutrition during bleaching?
colonies I did not conduct detailed recruitment sur-
veys during the bleaching event but visits to each The western side of Glovers Atoll experiences con-
study site suggested that approximately 25",, of re- tinual sedirnent deposition from the seaward lagoon
cruits showed either partial or (occasionally) full (Gischler 1994). Whilst sediment can reduce the
bleaching. These observations were made a third of growth rate, smother and kill juvenile corals (Birke-
the way into the bleaching event a n d cannot be con- land 1977, Hunte & Wittenberg 1992, Babcock &
sidered representative since a n unknown proportion of Mundy 1996), low levels of sediment may perrnit hete-
recruits may have bleached earlier and subsequently rotrophic feeding on epipelic micro-organisms (Toma-
recovered or died, or bleached later (the Same is true of scik & Sander 1987).Since the levels of suspcnded sed-
snapshot estimates of bleaching intensity in adult iment deposition at Glovers a r e not high enough to
corals). It is safest to conclude that at least 2 5 % of deem the reef uninhabitable to juvenile corals, it is fea-
recruits expenenced some bleaching during the event sible (but not tested) that sedimentation levels aug-
a n d that 1 mo after the adults had regained normal ment the feeding and therefore survivorship of recruits
colour only 1 "" of recruits exhibited even partial on this atoll.
bleach.ing. The difficulties of quantifying the severity
of the bleaching event notwithstanding, it appears
unlikely that recruits survived a bleaching event (4) Do juvenile corals receive less irradiance by virtue
purely by avoiding becoming bleached; it is more of their cryptic microhabitat?
likely that the incidence of bleaching in juvenile corals
was less than that in adults. It is not clear whether High levels of ultraviolet and photosynthetically
reduced bleaching in juvenile corals might result from active radiation (PAR) have been implicated to stimu-
a n ontogenic physiological change in zooxanthellate late coral bleaching (see review by Brown 1997).
susceptibility to bleaching, or simply a n external con- Whether the cryptic location of many juvenile corals
sequence of juvenile microhabitat (see suggestions on, for example, under-sides and vertical surfaces
under Question 4 below). (Babcock & Mundy 1996) confers a refuge from sus-
tained direct exposure to i.rradiance remains to be
Seen. Furtherrnore, whilst some juvenile corals bleach,
(2) Was bleaching-induced stress insufficient to create exposure of the (bleached) coral tissue to PAR may
colony mortality? partly determine the fate of the coral. Studies are
needed into the scattering and attenuation of irradi-
Did bleaching stress reduce growth rates effectively ance at the scales of recruit microhabitat and into the
shifting juveniles into a dormant state? Dormancy direct effects of irradiance on bleached coral tissue.
would help explain the consistent size-frequency dis-
tributions at Sites W1 and W2 before a n d after bleach-
ing, but for population Parameters to remain un- Effects of coral bleaching plus Hurricane Mitch
changed, chronic levels of mortality would have to be
absent or balanced by recruitment and growth. Mor- Coral bleaching was present throughout the Belize
tality rates are unlikely to be Zero over 6 mo (Bak & Barrier Reef and atolls making it impossible to distin-
Engel 1979) and therefore recruitment and growth guish the effects of hurricane disturbance on bleached
must have occurred. It is not clear whether mortality and non-bleached coral populations. Given the ob-
rates are simply low and balanced by low levels of served absence of a bleaching-induced disturbance to
recruitment and growth, or whether population sizes juvenile corals at western sites, however, it seems
a r e tightly regulated (e.g. by density-dependent mor- unlikely that bleaching would have significantly exac-
tality) such that even a marked mortality event could erbated the damage created by the hurricane. Hurri-34 Mar Ecol Prog Ser
cane events lead to mortality of recruits by sediment Canbbean reefs which also expenenced severe
scouring, direct mechanical breakage, and the re- bleaching. The responses of juvenile coral populations
moval of substratum. Post-hurncane events such as an to large-scale phenomena such as coral bleaching
ephemeral bloom of blue-green and filamentous green need to be categonsed. For each type of bleaching
algae (R. B. Aronson & T. J. Bnght pers. comm.) may event (e.g. duration, percent of adults affected in each
also create further stress: Van Moorsel (1985) found bleaching class), classifications should attempt to
filamentous algae to be the greatest cause of mortality relate the physical and biological conditions of the site
in juvenile Agancia humilis. (e.g. depth, physical exposure, herbivore grazing in-
Spatially patchy responses of adult cornmunities to tensity, adult coral cover) to the responses of juveniles
hurncane damage are weli established (Woodley et al. at the scales of comrnunity, life history strategy, and
1981, Edmunds & Witrnan 1991, Witman 1992, Bythell individual populations. If patterns emerge at large spa-
et al. 1993a,b,Rogers 1993),and, based on this study, it tial scales, such classifications will be instrumental in
appears that this premise extends to juvenile commu- modelling the irnpacts of bleaching events on the
nities at a depth of 8 to 10 m. The proportional reduc- dynamics of coral metapopulations (Mumby 1999) and
tion of Agancia and Leptoseris recruits was less at Site therefore help bndge the gap between the large scale
E1 than Site E2. Site-specific mortality patterns may of many population processes and the often inade-
offer a simple explanation of the differences in relative quate scale at which they are studied.
agancid abundance. First, survivorship of agancid
recruits may have been higher at Site E1 because the
cover of Montastraea was greater at Site E1 (ca 60 % vs Acknowledgements. I would iike to thank Elizabeth Glynn,
Ben Hadfield, and Karen Jarnes for their assistance in the
39% at Site E2; note cover of Montastraea is excep-
field. Dr Tom Bright, Cindy Liles, and the staff of Glovers Reef
tionally high at these sites). Most agancid recruits sur- Marine Research Station provided invaluable logistical sup-
veyed in January were found deep between Montas- port. I thank the Belize Departrnent of Fisheries and the
traea knobs, which may have provided shelter from Wildlife Conservation Society for permission to work at
scouring and direct mechanical stress. Second, prox- Glovers A t d . The comments of 4 referees improved a n ear-
Lier version o m e manuscript. This study was funded by a
irnity to reef cuts may affect the velocity and surge of NERC Fellowship under the Earth Observation Science Initia-
water. Site E1 is near a reef cut whereas Site E2 is mid- tive. This is contribution number 5 of Glovers Reef Marine
way along a continuous reef (Fig. 1).Mechanical dam- Research Station.
age to adult colonies appeared to be more severe at
Site E2, which might be because dispersal of stornl
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Editorial responsibility: Otto Kinne (Editor), Subrnitted: March 15, 1999; Accepted: July 16, 1999
Oldendorf/Luhe, Germany Proofs received from author(s): November 25, 1999You can also read
