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Burke et al 04
Hydrobiologia 530/531: 481–487, 2004.
D.G. Fautin, J.A. Westfall, P. Cartwright, M. Daly & C.R. Wyttenbach (eds), 481
Coelenterate Biology 2003: Trends in Research on Cnidaria and Ctenophora.
Ó 2004 Kluwer Academic Publishers. Printed in the Netherlands.
Coral mortality, recovery and reef degradation at Mexico Rocks Patch Reef
Complex, Northern Belize, Central America: 1995–1997
C.D. Burke1,*, T.M. McHenry2, W.D. Bischoff1, E.S. Huttig1, W. Yang1 & L. Thorndyke1
1
Department of Geology, Wichita State University, Wichita, KS 67260-0027, USA
2
Levine-Fricke, 316 N. Ridgewood, Wichita, KS 67208, USA
(*Author for correspondence: Tel.: +1-316-978-3140, Fax: +1-316-978-7229, E-mail: collette.burke@wichita.edu)
Key words: biotic phase shift
Abstract
The 1995 coral bleaching event in the western Caribbean was the first reported episode that significantly
affected the Belize barrier and lagoonal patch reefs. Bleaching was attributed to a 2 mo period of warm
water temperatures above 30 °C. Near Ambergris Caye, barrier and patch reefs experienced up to 50%
bleaching. At Mexico Rocks patch reef complex, the bleaching resulted in changes in reef health, com-
munity, and physical structure. Prior to the hyperthermal episode, patch reef surface area consisted of 47%
healthy framework coral coverage, 12% secondarily colonized biotic coverage, 35% dead coral surfaces that
were degraded by biological activity and physical erosion, and 6% cavities. six months after bleaching, most
corals had regained their color, but, owing to coral mortality, areas of surface degradation had increased to
an average 49% (p ¼ 0.029 based on Kruskal–Wallis analyses). Eighteen months after bleaching, degraded
surface areas expanded to 53% ( p ¼ 0.0366). Although re-coloring indicates rapid recovery for surviving
corals, the persistence in dead coral surfaces suggests that reef skeletal structure recovery lags behind that of
individual corals. Initial results of framework measurements indicate that bleaching events may result in an
ÔimbalanceÕ in the carbonate production rate of coral reefs and produce mass wasting of the skeletal
structure. Remapping of reef skeletal structure should establish quantitative measures for the long-term
effects of bleaching on patch reef frameworks.
Introduction northern Belize, was severely affected by this
thermal episode, when surface water temperatures
Coral bleaching as a result of higher than average in the shallow back-reef area in northern Belize
water temperatures commonly has been associated increased to 32–34 °C (Sprowls, 1995). Aerial and
with El Nino/Southern Oscillation events as re- underwater surveys of the bleaching event indi-
ported in the Pacific in 1982–1983, 1987, and 1998 cated that as much as 50% of the corals were
(Glynn, 1988a, 1993; Viets, 1998). Elevated sea bleached both at Mexico Rocks and on the barrier
surface temperatures in the western Atlantic from reef (CARICOMP, 1997). This paper presents the
August through October 1995 also produced effects of the 1995 bleaching episode at the Mexico
widespread bleaching of corals from the Belize Rocks patch reefs, summarizes short-term coral
barrier and lagoonal patch reefs (Holden, 1995; recovery since that time, and describes long-term
CARICOMP, 1997). This event marked the first effects on patch reef skeletal structure.
documented coral bleaching in this area (Stout, Bleaching occurs when stony corals lose
1995). The Mexico Rocks patch reef complex, or expel all or a portion of their endosymbionts
located 0.3 km seaward of Ambergris Caye in (zooxanthellae). Several factors have been impli-
482
cated for this disruptive process, including disease are about 2.1 m high and have grown to within
(Kushmaro et al., 1966; Gleason & Wellington, 0.5 m of mean sea level. The patch reefs have
1993; Ritchie et al., 1993), increased UV radiation grown atop and on the flanks of a narrow,
flux (Jokiel & York, 1984), hyposalinity (Good- northeast-trending ridge of karsted Pleistocene
body, 1961; Goreau, 1964), increased sediment limestone. Growth was initiated during the Flan-
flux (Acevedo & Goenaga, 1986), pollution (Neff drian transgression at about 3.5 Ka ago (Mazzullo
& Anderson, 1981), and temperature increases, et al., 1992, 1993; Burke et al., 1998).
some of which are possibly associated with global Water depths immediately around the complex
warming (Jokiel & Coles, 1990; Glynn, 1991, 1993; and between patch reefs average 2.7 m, and
Smith & Buddemeier, 1992). increase to about 4 m in a seaward direction be-
The ability of corals to recover their zooxan- fore shallowing to about 0.9 m toward the barrier
thellae after bleaching appears to be species-spe- reef flat. Temperature, salinity, and pH were re-
cific and related to their susceptibility to increases corded at least once a year within and around the
in water temperature, and recovery period can complex over the period from 1988 to 1998.
range from months to years (Hays & Bush, 1990; Salinity of the water is constant at 38&, and
Holden, 1995). Research on bleached and then daytime pH ranges from 8.0 to 8.4. Average daily
recovered Montastrea annularis in reefs in the surface ocean temperatures range seasonally from
Cayman Islands, for example, indicates that heal- 27 to 29 °C. The semi-diurnal tidal range is less
ing is gradual, and involves acquisition of a new than 0.5 m and typical wave energy, which is
population of zooxanthellae and restoration of qualitatively characterized as moderate (except
their densities to normal, non-bleached levels during storms or unusually calm weather), is dri-
(Hays & Bush, 1990). Additional consequences of ven by onshore and seasonal easterly trade winds
bleaching include decreased skeletal growth, re- and, to a lesser extent, by tides. Some wave energy
pressed gonad growth and reproduction, increased is input through passes in the barrier reef.
predation pressure on surviving corals, and in-
creased mortality (Jokiel & Coles, 1977, 1984;
Glynn, 1988b, 1990, 1993; Hughes, 1989; Brown & Methods
Suharsono, 1990; Goreau & MacFarlane, 1990;
Szmant & Gassman, 1990). Occasional reports of Twenty-three patch reefs ranging from 4 to 370 m2
framework deterioration have also been reported were geologically mapped and biologically sur-
(Glynn, 1988b, 1993; Eakin, 1991). veyed (using line transect and area measurements)
in 1990 for determination of coral–algal coverage,
percentage of dead coral (herein called areas of
Study area degradation), percentage of cavities, and both
linear and vertical dimensions of each patch reef
Mexico Rocks patch reef complex is located on the framework (cf. Burke et al., 1998 for specific field
outer shelf platform offshore of northern Belize, methods and survey results). A rope line, cali-
about 0.3 km seaward of Ambergris Caye, and brated at meter intervals, was placed along the
0.4 km to the lee of the platform-margin barrier long axis of each of the 23 selected reefs. At each
reef. Dimensions of the complex are approxi- meter section, both area measurements of biotic
mately 1.7 km in length and 0.5 km in width. It coverage, degradation and cavities, and the biota
has been under consideration for preserve status beneath the rope line were recorded on underwater
by the Belize government, and has been the site of slates for the length of each patch reef. A steel
baseline research by the authors since 1988 reinforcement bar calibrated at 0.3 m intervals was
(Mazzullo et al., 1992, 1993; McHenry, 1996; used for field measurements of horizontal and
Burke et al., 1998). The complex includes vertical dimensions at each meter interval along
approximately 100 individual patch reefs, which the rope line. Horizontal measurements included
consist predominantly of the Montastrea annularis the width of each meter section along the length of
complex of coral heads that range in area from the patch reef in meters. At each 1 m interval,
approximately 4–400 m2. The largest of these reefs vertical measurements were taken at the center of
483
the reef, and at least two locations perpendicular
to the long axis. This resulted in a minimum of
three vertical measurements for each meter section
across the top and flanks of each patch reef. To
assure good correspondence between reef topog-
raphy and contour mapping, wide or cavernous
reefs required additional height measurements. All
dimensional measurements from each patch reef
were used to construct contour maps of each patch
that also serve as base maps for annual monitoring
of reef health. Yearly assessment of coral–algal
coverage, percentage of dead coral, percentage of
cavities on the reef surface, and changes in
dimensions of the patch reefs, can be compared to
these original base maps for each of the 23 patch Figure 1. Patch reef composition. Weighted percentage by area
reefs. This field technique provides a method to of coral and non-coral biotic coverage, degradation, and sur-
monitor the health of reef skeletal structure. An face cavities at the Mexico Rocks patch reef complex, 1988–
estimate of framework erosion can be determined 1997.
by comparing original base maps to annual
assessments of surface area degradation and cavi-
ties present as well as to vertical distance below Degraded areas on the framework resulting
mean sea level to the tops of the colonies. These from biological and physical erosion averaged 35%
data can be useful for monitoring long term, of measured reef surface area (Fig. 1). Additional
temporal changes in the skeletal framework and coral species (e.g., Agaracia spp., Acropora spp.,
coral coverage on patch reefs, or any section of and Porities spp.) and, locally, calcareous algae
any reef. (e.g., Halimeda spp. and Amphiroa spp.), filamen-
tous (turf) algae, and macro algae (e.g., Padina and
Turbinaria) or encrusting and boring sponges,
Results and discussion colonized these areas of dead coral, thereby
increasing species richness on the patch reefs and
Pre-bleached parameters comprising 12% of biotic coverage (Mazzullo et al.,
1992, 1993; McHenry, 1996; Burke et al., 1998).
Prior to the 1995 hyperthermal episode, patch reef The distribution of non-scleractinid coral biota was
surface area consisted of 47% healthy stony coral controlled by the amount and distribution of sur-
coverage, 10% soft coral/sponge coverage, 2% al- face degradation and cavities (Burke et al., 1998).
gae, 35% dead coral surfaces that were degraded Commonly, localized growths of non-calcifying
by biological activity and physical erosion, and 6% macro algae, turf algae, and encrusting sponges
cavities (Fig. 1). On the 23 measured patch reefs, were restricted to large, degraded patch reefs, and
the head corals Montastrea annularis (sensu strictu) were rarely found growing on medium or small
composed 83%, and Diploria spp. and Dichocoenia patch reefs with little degradation. Calcareous al-
sp. together composed 1% of total area of living gae and non-encrusting sponges grew in degraded
reef-framework biota (coral species coverage). regions among lobes of corals and skeletal cavities.
Other species of Montastrea (e.g., faveolata, Cavities on the patch reefs averaged 6% of the
franksi, and cavernosa) were observed in the complex (Fig. 1). Most of the medium and small
complex, but were localized, and did not constitute clusters of head corals contained few cavities; lar-
a noteworthy portion of the measured patch reefs ger patch reefs generally contained larger cavities.
or of the complex. The remaining 16% of corals Because of the dominance of head corals, the reefs
consisted of Agaricia spp., Porites spp., Acropora were clustered domes that had coalesced over time
spp., and other branching scleractinids; and reef- and grown to within 0.5 m of sea level. No sig-
dwelling Millepora spp. nificant changes in the geometric shapes of the
484
patch reefs, heights below mean sea level, species tion (cf. Jokiel & Coles, 1977; Glynn, 1988a, 1993;
coverage, degraded areas, and extent of cavities Hughes, 1989; Brown & Suharsono, 1990; Goreau
were noted from 1988 to 1993 (Burke et al., 1998). & Macfarlane, 1990; Szmant & Gassman, 1990;
In fact, the 23 patch reefs in the complex were McCook, 1999).
easily identifiable from year to year based upon Increase in standing crop of algae indicates a
these attributes. phase shift in biotic distribution on the reefs. Most
of the degraded surfaces at Mexico Rocks had
Post-bleaching parameters – 1996 been colonized extensively, and in some cases,
entire reefs were nearly overgrown, by noncalci-
Increase in degradation, shift in species distribution, fying turf algae. To further complicate recovery,
and presence of diseased corals macro-algae, including intertwining mats of
The patch reefs were re-surveyed in March 1996, Caulerpa racemosa and meadows of Turbinaria
6 mo after the 1995 bleaching event. Evidence of spp. and Padina spp. covered the patch reef sur-
active bleaching was minimal: less than 1% of the faces. Before 1996 these algae were restricted to
corals were bleached. Most of the previously large, degraded portions of reefs in the complex. In
whitened corals had regained their normal color, 1996, nearly all the patch reefs supported macro-
and presumably, their population of zooxanthel- algae, and in some cases, entire reefs were nearly
lae. Rapid recovery of surviving corals after the overgrown by Caulerpa racemosa. This increase in
bleaching event therefore is indicated. macroalgal abundance may have resulted from
To determine the extent of coral survival, we coral mortality, corals weakened by bleaching with
re-measured the area of degraded reef framework. inhibited natural chemical and physical defense
Dead reef surfaces had increased on average to systems (cf. Lang, 1973), and lack of algal her-
49% of the reef frameworks (Figs 1 and 2). This bivory. As a consequence, algal standing crop in-
significant increase ( p ¼ 0.029 based on Kruskal– creased, and resulted in a dramatic phase shift in
Wallis analyses) was the result of coral mortality reef biotic distribution (cf. Jokiel & Coles, 1977;
and indicates that the 1995 Caribbean bleaching Glynn, 1988a, 1993; Hughes, 1989; 1994; Brown &
event resulted in significant coral mortality on Suharsono, 1990; Goreau & Macfarlane, 1990;
these patch reefs within 6 months. Most of these Szmant & Gassman, 1990; McCook, 1999).
ÔnewÕ zones of degradation were already colonized Coral bleaching has been implicated in the
by algae, a phenomena that is noted by many suppression of normal coral physiology including
Pacific reef workers as a post-bleaching ramifica- carbonate secretion (Glynn, 1993). The increase in
PATCH REEF DEGRADATION
Figure 2. Patch reef degradation. Percentage of patch reef surface area degraded in 1988–1993, 1996, and 1997. Solid black bar is area
degraded prior to bleaching (1993). Solid white bar is area degraded in 1996, 6 months after bleaching. Gray bar is area degraded in
1997, 18 mo after bleaching. The degraded surface area on the patch reefs increased significantly after the 1995 bleaching event.
485
dead reef surfaces may reflect these physiological 13, located in the northern portion of the complex.
complications. For example, corals weakened by In 1993, mapping of this patch reef indicated that
bleaching may be unable to ward off pathogens the total volume of the framework was 26 m3. Re-
or disease epizooids that ultimately lead to coral mapping of the patch reef in 1997 indicated that
mortality. As noted by Glynn (1993, p. 5), incre- the total volume of the reef was 24 m3 which
ases in coral diseases may be a result of stressors represents an approximate loss of about 2 m3 of
placed on corals by bleaching. carbonate. This decrease in volume was attribut-
By March, 1996, previously unrecorded coral able to reduction in the height of the reef below
diseases such as White Plague and Pox were mean sea level. In essence, the large domed Mon-
present on the reefs, but were sufficiently uncom- tastrea annularis head that comprised the reef
mon to warrant a category on survey transects. framework had collapsed, and produced an
Evidence of white band and plague diseases were erratically cratered reef topography. Similar signs
present in the form of fresh white spotting of coral of mass wasting were present throughout the
surfaces that were devoid of living corals. Black complex such that patch reefs easily recognizable
band disease was also present, but has been a through geometric shape by the authors in previ-
persistent, contained disease in the complex for ous years were unrecognizable except by map
many years. location in 1997. A study to quantify the signifi-
cance of this carbonate loss is underway.
Post-bleaching – 1997
Increase in degradation and change in patch reef Conclusion
geometry
The patch reefs were again resurveyed in 1997, Although reports on global coral health suggest
18 mo after the bleaching event. At this time, less that coral reefs remotely located away from cen-
than 1% of the corals, including the dominant ters of human population are not deteriorating
frame builder, Montastrea annularis (sensu strictu), (Pennisi, 1997), near shore reefs like Mexico Rocks
displayed signs of active bleaching. An ÔapparentÕ are more typical of the patch reefs associated with
shift in morphotypes to M. franksi was noted but increasing eco-tourism, harvesting, and onshore
not quantified on several reefs. Localized areas of development. Conditions here are generally well
diseased corals were present in the complex as in disposed for reef growth; however, lagoonal patch
the previous year. reefs at Mexico Rocks are subjected to more var-
The average amount of surface degraded area, iable environmental conditions and anthropogenic
however, had increased from 49% to 53% in 1996. stresses because of their proximity to shore than
This increase in degraded areas from 1996 to 1997 are remotely located reefs. These shallow water
(Fig. 1) is statistically significant ( p ¼ 0.0366), and patch reefs were among the first to succumb to
suggests that coral mortality continued to occur bleaching, and their recovery time was slower than
throughout 1996–1997. Based upon these results, those corals that comprise the barrier reef (CAR-
several implications can be made. First, re-color- ICOMP, 1997).
ation of corals is only a partial measure of reef At Mexico Rocks, the sequence of post-
recovery and occurs rapidly after waters cool. bleaching events that was observed on the patch
Secondly, recovery of the reef framework lags be- reefs includes (1) significant increase in coral
hind that of individual corals, and may be at risk mortality as indicated by dead coral surface cov-
because fewer corals are producing calcium car- erage and diseased corals, (2) phase shift in biotic
bonate due to coral mortality. Evidence for distribution, and (3) initial deterioration of reef
framework decline was present by 1997. framework. Re-coloration of surviving corals
Patch Reefs 15 and 7 (87.7 and 4.2 m2 in area, developed soon after waters began to cool. Dete-
respectively), which are located in different areas rioration of reef frameworks, however, may be a
of the complex, had collapsed and all but disap- long-term process.
peared (Fig. 2). A less dramatic, but typical Based on radiocarbon age dates, patch reefs at
example of skeletal structure collapse is patch reef Mexico Rocks have grown and diversified for
486
hundreds of years (Burke et al., 1998). In contrast, Glynn, P. W., 1990. Coral mortality and disturbances to coral
only a few years were required to initiate reef reefs in the tropical eastern Pacific. In Glynn, P. W. (ed.),
deterioration after living reefs were subjected to a Global Ecological Consequences of the 1982–83 El Nino- ˜
Southern Oscillation. Elsevier, Amsterdam: 55–126.
severe bleaching event, the predictable results of Glynn, P. W., 1991. Coral bleaching in the 1980’s and possible
which were coral mortality and algal increase. connections with global warming. Trends in Ecology Evo-
When corals do not produce calcium carbonate lution 6: 175–179.
exceeding or in equilibrium with reef erosional Glynn, P. W., 1993. Coral reef bleaching: ecological perspec-
processes, reef skeletal structures may undergo tives. Coral Reefs 12: 1–17.
Goodbody, I., 1961. Mass mortality of marine fauna following
mass wasting by biological and physical degrada- tropical rain. Ecology 42: 150.
tion. Analogous reef skeletal structure demise was Goreau, T. F., 1964. Mass expulsion of zooxanthellae from
observed in the Pacific as a result of the 1982–1983 Jamaican reef communities after Hurricane Flora. Science
El Nino by Glynn (1988b, 1993) and Eakin (1991). 145: 383–386.
Further study of these patch reefs is necessary to Goreau, T. J. & A. H. MacFarlane, 1990. Reduced growth rate
of Montastrea annularis following the 1987–1988 coral
determine the significance and permanency of bleaching event. Coral Reefs 8: 211–215.
framework mass wasting. Hays, R. L. & P. G. Bush, 1990. Microscopic observations of
recovery of the reef-building scleractinian coral, Montastrea
annularis, after bleaching on a Cayman reef. Coral Reefs 8:
Acknowledgments 203–209.
Holden, C., 1995. Reef bleaching spreads in Caribbean. Science
270: 919.
The authors would like to acknowledge the sup-
Hughes, T. P., 1989. Community structure and diversity of
port provided by the Belize Department of Fish- coral reefs: the role of history. Ecology 70: 275–279.
eries, Janet Gibson, James Azueta, Hol Chan, and Hughes, T. P., 1994. Catastrophes, phase shifts and large-scale
Bacalar Chico Marine Preserves for the boat time degradation of a Caribbean coral reef. Science 265: 1547–1551.
and long-term logistical support necessary to Jokiel, P. L. & S. J. Coles, 1977. Effects of temperature on the
accomplish this research, without which, the work mortality and growth of Hawaiian reef corals. Marine
Biology 43: 201–208.
would not have been completed. Jokiel, P. L. & S. J. Coles, 1990. Response of Hawaii and other
Indo-Pacific reef corals to elevated temperature. Coral Reefs
8: 155–162.
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Gleason, D. F. & G. M. Wellington,1993. Ultraviolet radiation McHenry, T. M., 1996. Ecology of Mexico Rocks Modern Patch
and coral bleaching. Nature 365: 836–838. Reef Complex, Belize, Central America. Master Science
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D.G. Fautin, J.A. Westfall, P. Cartwright, M. Daly & C.R. Wyttenbach (eds), 481
Coelenterate Biology 2003: Trends in Research on Cnidaria and Ctenophora.
Ó 2004 Kluwer Academic Publishers. Printed in the Netherlands.
Coral mortality, recovery and reef degradation at Mexico Rocks Patch Reef
Complex, Northern Belize, Central America: 1995–1997
C.D. Burke1,*, T.M. McHenry2, W.D. Bischoff1, E.S. Huttig1, W. Yang1 & L. Thorndyke1
1
Department of Geology, Wichita State University, Wichita, KS 67260-0027, USA
2
Levine-Fricke, 316 N. Ridgewood, Wichita, KS 67208, USA
(*Author for correspondence: Tel.: +1-316-978-3140, Fax: +1-316-978-7229, E-mail: collette.burke@wichita.edu)
Key words: biotic phase shift
Abstract
The 1995 coral bleaching event in the western Caribbean was the first reported episode that significantly
affected the Belize barrier and lagoonal patch reefs. Bleaching was attributed to a 2 mo period of warm
water temperatures above 30 °C. Near Ambergris Caye, barrier and patch reefs experienced up to 50%
bleaching. At Mexico Rocks patch reef complex, the bleaching resulted in changes in reef health, com-
munity, and physical structure. Prior to the hyperthermal episode, patch reef surface area consisted of 47%
healthy framework coral coverage, 12% secondarily colonized biotic coverage, 35% dead coral surfaces that
were degraded by biological activity and physical erosion, and 6% cavities. six months after bleaching, most
corals had regained their color, but, owing to coral mortality, areas of surface degradation had increased to
an average 49% (p ¼ 0.029 based on Kruskal–Wallis analyses). Eighteen months after bleaching, degraded
surface areas expanded to 53% ( p ¼ 0.0366). Although re-coloring indicates rapid recovery for surviving
corals, the persistence in dead coral surfaces suggests that reef skeletal structure recovery lags behind that of
individual corals. Initial results of framework measurements indicate that bleaching events may result in an
ÔimbalanceÕ in the carbonate production rate of coral reefs and produce mass wasting of the skeletal
structure. Remapping of reef skeletal structure should establish quantitative measures for the long-term
effects of bleaching on patch reef frameworks.
Introduction northern Belize, was severely affected by this
thermal episode, when surface water temperatures
Coral bleaching as a result of higher than average in the shallow back-reef area in northern Belize
water temperatures commonly has been associated increased to 32–34 °C (Sprowls, 1995). Aerial and
with El Nino/Southern Oscillation events as re- underwater surveys of the bleaching event indi-
ported in the Pacific in 1982–1983, 1987, and 1998 cated that as much as 50% of the corals were
(Glynn, 1988a, 1993; Viets, 1998). Elevated sea bleached both at Mexico Rocks and on the barrier
surface temperatures in the western Atlantic from reef (CARICOMP, 1997). This paper presents the
August through October 1995 also produced effects of the 1995 bleaching episode at the Mexico
widespread bleaching of corals from the Belize Rocks patch reefs, summarizes short-term coral
barrier and lagoonal patch reefs (Holden, 1995; recovery since that time, and describes long-term
CARICOMP, 1997). This event marked the first effects on patch reef skeletal structure.
documented coral bleaching in this area (Stout, Bleaching occurs when stony corals lose
1995). The Mexico Rocks patch reef complex, or expel all or a portion of their endosymbionts
located 0.3 km seaward of Ambergris Caye in (zooxanthellae). Several factors have been impli-
482
cated for this disruptive process, including disease are about 2.1 m high and have grown to within
(Kushmaro et al., 1966; Gleason & Wellington, 0.5 m of mean sea level. The patch reefs have
1993; Ritchie et al., 1993), increased UV radiation grown atop and on the flanks of a narrow,
flux (Jokiel & York, 1984), hyposalinity (Good- northeast-trending ridge of karsted Pleistocene
body, 1961; Goreau, 1964), increased sediment limestone. Growth was initiated during the Flan-
flux (Acevedo & Goenaga, 1986), pollution (Neff drian transgression at about 3.5 Ka ago (Mazzullo
& Anderson, 1981), and temperature increases, et al., 1992, 1993; Burke et al., 1998).
some of which are possibly associated with global Water depths immediately around the complex
warming (Jokiel & Coles, 1990; Glynn, 1991, 1993; and between patch reefs average 2.7 m, and
Smith & Buddemeier, 1992). increase to about 4 m in a seaward direction be-
The ability of corals to recover their zooxan- fore shallowing to about 0.9 m toward the barrier
thellae after bleaching appears to be species-spe- reef flat. Temperature, salinity, and pH were re-
cific and related to their susceptibility to increases corded at least once a year within and around the
in water temperature, and recovery period can complex over the period from 1988 to 1998.
range from months to years (Hays & Bush, 1990; Salinity of the water is constant at 38&, and
Holden, 1995). Research on bleached and then daytime pH ranges from 8.0 to 8.4. Average daily
recovered Montastrea annularis in reefs in the surface ocean temperatures range seasonally from
Cayman Islands, for example, indicates that heal- 27 to 29 °C. The semi-diurnal tidal range is less
ing is gradual, and involves acquisition of a new than 0.5 m and typical wave energy, which is
population of zooxanthellae and restoration of qualitatively characterized as moderate (except
their densities to normal, non-bleached levels during storms or unusually calm weather), is dri-
(Hays & Bush, 1990). Additional consequences of ven by onshore and seasonal easterly trade winds
bleaching include decreased skeletal growth, re- and, to a lesser extent, by tides. Some wave energy
pressed gonad growth and reproduction, increased is input through passes in the barrier reef.
predation pressure on surviving corals, and in-
creased mortality (Jokiel & Coles, 1977, 1984;
Glynn, 1988b, 1990, 1993; Hughes, 1989; Brown & Methods
Suharsono, 1990; Goreau & MacFarlane, 1990;
Szmant & Gassman, 1990). Occasional reports of Twenty-three patch reefs ranging from 4 to 370 m2
framework deterioration have also been reported were geologically mapped and biologically sur-
(Glynn, 1988b, 1993; Eakin, 1991). veyed (using line transect and area measurements)
in 1990 for determination of coral–algal coverage,
percentage of dead coral (herein called areas of
Study area degradation), percentage of cavities, and both
linear and vertical dimensions of each patch reef
Mexico Rocks patch reef complex is located on the framework (cf. Burke et al., 1998 for specific field
outer shelf platform offshore of northern Belize, methods and survey results). A rope line, cali-
about 0.3 km seaward of Ambergris Caye, and brated at meter intervals, was placed along the
0.4 km to the lee of the platform-margin barrier long axis of each of the 23 selected reefs. At each
reef. Dimensions of the complex are approxi- meter section, both area measurements of biotic
mately 1.7 km in length and 0.5 km in width. It coverage, degradation and cavities, and the biota
has been under consideration for preserve status beneath the rope line were recorded on underwater
by the Belize government, and has been the site of slates for the length of each patch reef. A steel
baseline research by the authors since 1988 reinforcement bar calibrated at 0.3 m intervals was
(Mazzullo et al., 1992, 1993; McHenry, 1996; used for field measurements of horizontal and
Burke et al., 1998). The complex includes vertical dimensions at each meter interval along
approximately 100 individual patch reefs, which the rope line. Horizontal measurements included
consist predominantly of the Montastrea annularis the width of each meter section along the length of
complex of coral heads that range in area from the patch reef in meters. At each 1 m interval,
approximately 4–400 m2. The largest of these reefs vertical measurements were taken at the center of
483
the reef, and at least two locations perpendicular
to the long axis. This resulted in a minimum of
three vertical measurements for each meter section
across the top and flanks of each patch reef. To
assure good correspondence between reef topog-
raphy and contour mapping, wide or cavernous
reefs required additional height measurements. All
dimensional measurements from each patch reef
were used to construct contour maps of each patch
that also serve as base maps for annual monitoring
of reef health. Yearly assessment of coral–algal
coverage, percentage of dead coral, percentage of
cavities on the reef surface, and changes in
dimensions of the patch reefs, can be compared to
these original base maps for each of the 23 patch Figure 1. Patch reef composition. Weighted percentage by area
reefs. This field technique provides a method to of coral and non-coral biotic coverage, degradation, and sur-
monitor the health of reef skeletal structure. An face cavities at the Mexico Rocks patch reef complex, 1988–
estimate of framework erosion can be determined 1997.
by comparing original base maps to annual
assessments of surface area degradation and cavi-
ties present as well as to vertical distance below Degraded areas on the framework resulting
mean sea level to the tops of the colonies. These from biological and physical erosion averaged 35%
data can be useful for monitoring long term, of measured reef surface area (Fig. 1). Additional
temporal changes in the skeletal framework and coral species (e.g., Agaracia spp., Acropora spp.,
coral coverage on patch reefs, or any section of and Porities spp.) and, locally, calcareous algae
any reef. (e.g., Halimeda spp. and Amphiroa spp.), filamen-
tous (turf) algae, and macro algae (e.g., Padina and
Turbinaria) or encrusting and boring sponges,
Results and discussion colonized these areas of dead coral, thereby
increasing species richness on the patch reefs and
Pre-bleached parameters comprising 12% of biotic coverage (Mazzullo et al.,
1992, 1993; McHenry, 1996; Burke et al., 1998).
Prior to the 1995 hyperthermal episode, patch reef The distribution of non-scleractinid coral biota was
surface area consisted of 47% healthy stony coral controlled by the amount and distribution of sur-
coverage, 10% soft coral/sponge coverage, 2% al- face degradation and cavities (Burke et al., 1998).
gae, 35% dead coral surfaces that were degraded Commonly, localized growths of non-calcifying
by biological activity and physical erosion, and 6% macro algae, turf algae, and encrusting sponges
cavities (Fig. 1). On the 23 measured patch reefs, were restricted to large, degraded patch reefs, and
the head corals Montastrea annularis (sensu strictu) were rarely found growing on medium or small
composed 83%, and Diploria spp. and Dichocoenia patch reefs with little degradation. Calcareous al-
sp. together composed 1% of total area of living gae and non-encrusting sponges grew in degraded
reef-framework biota (coral species coverage). regions among lobes of corals and skeletal cavities.
Other species of Montastrea (e.g., faveolata, Cavities on the patch reefs averaged 6% of the
franksi, and cavernosa) were observed in the complex (Fig. 1). Most of the medium and small
complex, but were localized, and did not constitute clusters of head corals contained few cavities; lar-
a noteworthy portion of the measured patch reefs ger patch reefs generally contained larger cavities.
or of the complex. The remaining 16% of corals Because of the dominance of head corals, the reefs
consisted of Agaricia spp., Porites spp., Acropora were clustered domes that had coalesced over time
spp., and other branching scleractinids; and reef- and grown to within 0.5 m of sea level. No sig-
dwelling Millepora spp. nificant changes in the geometric shapes of the
484
patch reefs, heights below mean sea level, species tion (cf. Jokiel & Coles, 1977; Glynn, 1988a, 1993;
coverage, degraded areas, and extent of cavities Hughes, 1989; Brown & Suharsono, 1990; Goreau
were noted from 1988 to 1993 (Burke et al., 1998). & Macfarlane, 1990; Szmant & Gassman, 1990;
In fact, the 23 patch reefs in the complex were McCook, 1999).
easily identifiable from year to year based upon Increase in standing crop of algae indicates a
these attributes. phase shift in biotic distribution on the reefs. Most
of the degraded surfaces at Mexico Rocks had
Post-bleaching parameters – 1996 been colonized extensively, and in some cases,
entire reefs were nearly overgrown, by noncalci-
Increase in degradation, shift in species distribution, fying turf algae. To further complicate recovery,
and presence of diseased corals macro-algae, including intertwining mats of
The patch reefs were re-surveyed in March 1996, Caulerpa racemosa and meadows of Turbinaria
6 mo after the 1995 bleaching event. Evidence of spp. and Padina spp. covered the patch reef sur-
active bleaching was minimal: less than 1% of the faces. Before 1996 these algae were restricted to
corals were bleached. Most of the previously large, degraded portions of reefs in the complex. In
whitened corals had regained their normal color, 1996, nearly all the patch reefs supported macro-
and presumably, their population of zooxanthel- algae, and in some cases, entire reefs were nearly
lae. Rapid recovery of surviving corals after the overgrown by Caulerpa racemosa. This increase in
bleaching event therefore is indicated. macroalgal abundance may have resulted from
To determine the extent of coral survival, we coral mortality, corals weakened by bleaching with
re-measured the area of degraded reef framework. inhibited natural chemical and physical defense
Dead reef surfaces had increased on average to systems (cf. Lang, 1973), and lack of algal her-
49% of the reef frameworks (Figs 1 and 2). This bivory. As a consequence, algal standing crop in-
significant increase ( p ¼ 0.029 based on Kruskal– creased, and resulted in a dramatic phase shift in
Wallis analyses) was the result of coral mortality reef biotic distribution (cf. Jokiel & Coles, 1977;
and indicates that the 1995 Caribbean bleaching Glynn, 1988a, 1993; Hughes, 1989; 1994; Brown &
event resulted in significant coral mortality on Suharsono, 1990; Goreau & Macfarlane, 1990;
these patch reefs within 6 months. Most of these Szmant & Gassman, 1990; McCook, 1999).
ÔnewÕ zones of degradation were already colonized Coral bleaching has been implicated in the
by algae, a phenomena that is noted by many suppression of normal coral physiology including
Pacific reef workers as a post-bleaching ramifica- carbonate secretion (Glynn, 1993). The increase in
PATCH REEF DEGRADATION
Figure 2. Patch reef degradation. Percentage of patch reef surface area degraded in 1988–1993, 1996, and 1997. Solid black bar is area
degraded prior to bleaching (1993). Solid white bar is area degraded in 1996, 6 months after bleaching. Gray bar is area degraded in
1997, 18 mo after bleaching. The degraded surface area on the patch reefs increased significantly after the 1995 bleaching event.
485
dead reef surfaces may reflect these physiological 13, located in the northern portion of the complex.
complications. For example, corals weakened by In 1993, mapping of this patch reef indicated that
bleaching may be unable to ward off pathogens the total volume of the framework was 26 m3. Re-
or disease epizooids that ultimately lead to coral mapping of the patch reef in 1997 indicated that
mortality. As noted by Glynn (1993, p. 5), incre- the total volume of the reef was 24 m3 which
ases in coral diseases may be a result of stressors represents an approximate loss of about 2 m3 of
placed on corals by bleaching. carbonate. This decrease in volume was attribut-
By March, 1996, previously unrecorded coral able to reduction in the height of the reef below
diseases such as White Plague and Pox were mean sea level. In essence, the large domed Mon-
present on the reefs, but were sufficiently uncom- tastrea annularis head that comprised the reef
mon to warrant a category on survey transects. framework had collapsed, and produced an
Evidence of white band and plague diseases were erratically cratered reef topography. Similar signs
present in the form of fresh white spotting of coral of mass wasting were present throughout the
surfaces that were devoid of living corals. Black complex such that patch reefs easily recognizable
band disease was also present, but has been a through geometric shape by the authors in previ-
persistent, contained disease in the complex for ous years were unrecognizable except by map
many years. location in 1997. A study to quantify the signifi-
cance of this carbonate loss is underway.
Post-bleaching – 1997
Increase in degradation and change in patch reef Conclusion
geometry
The patch reefs were again resurveyed in 1997, Although reports on global coral health suggest
18 mo after the bleaching event. At this time, less that coral reefs remotely located away from cen-
than 1% of the corals, including the dominant ters of human population are not deteriorating
frame builder, Montastrea annularis (sensu strictu), (Pennisi, 1997), near shore reefs like Mexico Rocks
displayed signs of active bleaching. An ÔapparentÕ are more typical of the patch reefs associated with
shift in morphotypes to M. franksi was noted but increasing eco-tourism, harvesting, and onshore
not quantified on several reefs. Localized areas of development. Conditions here are generally well
diseased corals were present in the complex as in disposed for reef growth; however, lagoonal patch
the previous year. reefs at Mexico Rocks are subjected to more var-
The average amount of surface degraded area, iable environmental conditions and anthropogenic
however, had increased from 49% to 53% in 1996. stresses because of their proximity to shore than
This increase in degraded areas from 1996 to 1997 are remotely located reefs. These shallow water
(Fig. 1) is statistically significant ( p ¼ 0.0366), and patch reefs were among the first to succumb to
suggests that coral mortality continued to occur bleaching, and their recovery time was slower than
throughout 1996–1997. Based upon these results, those corals that comprise the barrier reef (CAR-
several implications can be made. First, re-color- ICOMP, 1997).
ation of corals is only a partial measure of reef At Mexico Rocks, the sequence of post-
recovery and occurs rapidly after waters cool. bleaching events that was observed on the patch
Secondly, recovery of the reef framework lags be- reefs includes (1) significant increase in coral
hind that of individual corals, and may be at risk mortality as indicated by dead coral surface cov-
because fewer corals are producing calcium car- erage and diseased corals, (2) phase shift in biotic
bonate due to coral mortality. Evidence for distribution, and (3) initial deterioration of reef
framework decline was present by 1997. framework. Re-coloration of surviving corals
Patch Reefs 15 and 7 (87.7 and 4.2 m2 in area, developed soon after waters began to cool. Dete-
respectively), which are located in different areas rioration of reef frameworks, however, may be a
of the complex, had collapsed and all but disap- long-term process.
peared (Fig. 2). A less dramatic, but typical Based on radiocarbon age dates, patch reefs at
example of skeletal structure collapse is patch reef Mexico Rocks have grown and diversified for
486
hundreds of years (Burke et al., 1998). In contrast, Glynn, P. W., 1990. Coral mortality and disturbances to coral
only a few years were required to initiate reef reefs in the tropical eastern Pacific. In Glynn, P. W. (ed.),
deterioration after living reefs were subjected to a Global Ecological Consequences of the 1982–83 El Nino- ˜
Southern Oscillation. Elsevier, Amsterdam: 55–126.
severe bleaching event, the predictable results of Glynn, P. W., 1991. Coral bleaching in the 1980’s and possible
which were coral mortality and algal increase. connections with global warming. Trends in Ecology Evo-
When corals do not produce calcium carbonate lution 6: 175–179.
exceeding or in equilibrium with reef erosional Glynn, P. W., 1993. Coral reef bleaching: ecological perspec-
processes, reef skeletal structures may undergo tives. Coral Reefs 12: 1–17.
Goodbody, I., 1961. Mass mortality of marine fauna following
mass wasting by biological and physical degrada- tropical rain. Ecology 42: 150.
tion. Analogous reef skeletal structure demise was Goreau, T. F., 1964. Mass expulsion of zooxanthellae from
observed in the Pacific as a result of the 1982–1983 Jamaican reef communities after Hurricane Flora. Science
El Nino by Glynn (1988b, 1993) and Eakin (1991). 145: 383–386.
Further study of these patch reefs is necessary to Goreau, T. J. & A. H. MacFarlane, 1990. Reduced growth rate
of Montastrea annularis following the 1987–1988 coral
determine the significance and permanency of bleaching event. Coral Reefs 8: 211–215.
framework mass wasting. Hays, R. L. & P. G. Bush, 1990. Microscopic observations of
recovery of the reef-building scleractinian coral, Montastrea
annularis, after bleaching on a Cayman reef. Coral Reefs 8:
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Holden, C., 1995. Reef bleaching spreads in Caribbean. Science
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The authors would like to acknowledge the sup-
Hughes, T. P., 1989. Community structure and diversity of
port provided by the Belize Department of Fish- coral reefs: the role of history. Ecology 70: 275–279.
eries, Janet Gibson, James Azueta, Hol Chan, and Hughes, T. P., 1994. Catastrophes, phase shifts and large-scale
Bacalar Chico Marine Preserves for the boat time degradation of a Caribbean coral reef. Science 265: 1547–1551.
and long-term logistical support necessary to Jokiel, P. L. & S. J. Coles, 1977. Effects of temperature on the
accomplish this research, without which, the work mortality and growth of Hawaiian reef corals. Marine
Biology 43: 201–208.
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Indo-Pacific reef corals to elevated temperature. Coral Reefs
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