Content uploaded by William F Precht
Author content
All content in this area was uploaded by William F Precht on Jan 07, 2016
Content may be subject to copyright.
Natural populations face impending changes in the
global climate to which they will have to acclimate or
adapt, or else perish. Their responses to climate change will
have widespread species-level and community-level conse-
quences, and a number of ecologists have predicted changes
in the composition and distribution of future ecosystems
(Fields et al. 1993). The fingerprint of global climate change
can be mapped via the response of species to changes in their
physiographic environmental settings. Hundreds of species
have responded to recent warming trends by expanding
their ranges to higher latitudes, as well as by changing the
timing and duration of their flowering, breeding, migration,
and other climate-related behaviors (Parmesan and Yohe
2003; Root et al. 2003).
Most predictions about the effects of global climate
change on coral reefs have been confined to temperature-
induced coral bleaching (Hoegh-Guldberg 1999; Walther
et al. 2002), rising sea levels (Graus and Macintyre 1998),
and changing ocean chemistry (Kleypas et al. 2001).
Recent reports establish the first example of range expan-
sion of a Caribbean coral genus towards the Poles, in
response to climatic warming. First, spatially extensive
thickets of the staghorn coral, Acropora cervicornis (Figure
1), were discovered off Fort Lauderdale in Broward
County, Florida in 1998 (Vargas-Ángel et al. 2004), where
they had not been observed during the 1970s and 1980s.
More recently, colonies of the elkhorn coral, Acropora
palmata, have been observed as far north as Pompano
Beach in northern Broward County (Precht pers obs;
Figure 2). Also, elkhorn coral was seen for the first time in
2002 on reefs of the Flower Garden Banks in the northern
Gulf of Mexico (S Bernhardt pers comm). The sudden
appearance of Caribbean acroporid corals well north of
their previously known extant range is associated with
decadal-scale increases in annual sea-surface temperature
(SST) in the western Atlantic (Hoegh-Guldberg 1999;
Levitus et al. 2000; Barnett et al. 2001).
Although one cannot prove directly that the recent
expansion of acroporid corals is related to the impacts of
climate change, fossil reefs in Florida provide an opportu-
nity to examine the response of coral reefs to past global
change, especially rapid changes in SST. Well-developed
fossil Holocene reefs situated at the latitudinal extremes of
reef development are juxtaposed with depauperate (low-
diversity) living coral assemblages. The fossil reefs provide
a baseline for understanding the response of reef systems
to fluctuating climates, as well as for predicting the future
response of coral reefs to global change.
307
© The Ecological Society of America www.frontiersinecology.org
REVIEWS REVIEWS REVIEWS
Climate flickers and range shifts of reef
corals
William F Precht1and Richard B Aronson2
Staghorn coral (Acropora cervicornis) and elkhorn coral (Acropora palmata), are important reef builders in
the Caribbean. In the early to middle Holocene (10 000–6000 years ago), when sea temperatures were
warmer than today, Acropora-dominated reefs were common along the east coast of Florida as far north as
Palm Beach County. The fossil record shows that the northern limits of these two cold-sensitive species
subsequently contracted to Biscayne Bay, south of Miami, apparently as a result of climatic cooling. This
response of the Acropora species to climate provides a context for interpreting recent shifts in their geo-
graphic distribution. Despite recent disease-induced mass mortalities throughout the Caribbean and west-
ern Atlantic, the two species are now re-expanding their ranges northward along the Florida Peninsula and
into the northern Gulf of Mexico, coincident with increasing sea temperatures. In the face of continued
global warming, the northernmost limit of this range expansion will ultimately be determined by a com-
bination of temperature and other physical constraints.
Front Ecol Environ 2004; 2(6): 307–314
1Ecological Sciences Program, PBS&J, 2001 NW 107th Avenue,
Miami, FL 33172 (bprecht@pbsj.com); 2Dauphin Island Sea Lab,
101 Bienville Boulevard, Dauphin Island, AL 36528
In a nutshell:
•The ranges of staghorn and elkhorn corals were more expan-
sive during the early to middle Holocene, when sea tempera-
tures in the western Atlantic were warmer than they are at pre-
sent
•These two coral species are currently expanding their geo-
graphic ranges northward along the Florida Peninsula and into
the northern Gulf of Mexico
•The range expansion appears to be related to warming sea tem-
peratures
•The continued northward expansion of the geographic ranges
of coral species should not be accompanied by temperature-
induced extinction at lower latitudes
•On the other hand, geographic shifts will not mitigate
expected ecological and economic losses resulting from the
reduced functions of tropical reef systems
Global change and coral reefs WF Precht and RB Aronson
One of the most startling aspects of the recent discovery
of flourishing northern populations of Acropora is related
to the overall poor condition of Caribbean reefs. Gardner
et al. (2003) used meta-analysis to assess the extent of
coral decline across the Caribbean since the 1970s. Their
study revealed that reefs from all sectors of the region were
badly affected. Disturbances of various kinds have been
invoked to explain the changing face of Caribbean reefs
over the past 25 years, and coral mortality, especially the
mortality of Acropora spp, has been a major driving force
in the transition (Aronson and Precht 2001). Many fac-
tors have been responsible for Acropora mortality, but
white-band disease, temperature stress, predation, and
hurricanes have all played key roles in reducing popula-
tions both locally and regionally. The
acroporids are among the most impor-
tant reef builders in the Caribbean, so
their loss has been a major reason that
Caribbean reefs have declined. In the
face of this massive mortality, the
recent range expansion of Acropora was
unexpected.
Effects of temperature
Reef-building hard corals (order Scler-
actinia) are distributed along a latitudi-
nal diversity gradient, with the highest
species richness in the tropics. The ori-
gin and maintenance of this pattern,
and especially its persistence through
time, are not completely understood,
but temperature has long been consid-
ered the main controlling factor on the
distribution of these species. The opti-
mum temperature for coral growth is
about 26° to 28°C. Low-temperature tolerances are not
well defined for corals, but early experiments documented
16°C as stressful to most species and showed that exposure
to temperatures below 15°C can result in mortality (see
Shinn 1989). The present-day global distribution of coral
reefs generally coincides with the 18°C monthly mini-
mum seawater isotherm (Buddemeier et al. 2004).
Coral reefs in the Florida Keys are at the northern limit
of reef growth in the Americas. Caribbean acroporids are
especially sensitive to cold water, and sustained low tem-
peratures associated with the passage of winter cold fronts
have caused episodic mass mortalities of staghorn and
elkhorn corals in Florida and the Bahamas (Precht and
Miller in press). Rapid diminution of generic diversity
northwards along the east coast of
Florida is due primarily to cold-tempera-
ture limitations (Porter and Tougas
2001). Although the 18°C isotherm is
the approximate boundary for reef
building in the western Atlantic, the
ranges of a number of reef-building
species extend further northwards along
the east coast due to the poleward
transport of warm water, via the Florida
Current (a southern segment of the Gulf
Stream), and to the Flower Garden
Banks in the northern Gulf of Mexico,
due to the influence of the warm Loop
Current. During the recent past, Fowey
Rocks, located southeast of Miami, was
the northern extent of reef growth dom-
inated by acroporids (Shinn et al. 1989;
Figures 3 and 4). Assemblages of scler-
actinians and gorgonians (soft corals)
were found north of Fowey Rocks, off
308
www.frontiersinecology.org © The Ecological Society of America
Figure 1. Underwater photograph showing luxuriant thickets of staghorn coral
(Acropora cervicornis) recently found off Ft Lauderdale, FL. This is approximately
50 km north of the previous known extant range of Caribbean acroporids.
Figure 2. Underwater photograph of the northernmost known colony of elkhorn coral
(Acropora palmata) in the western Atlantic, located off Pompano Beach, FL.
WF Precht and RB Aronson Global change and coral reefs
Broward and Palm Beach Counties, with acroporid corals
generally being rare (staghorn coral) or absent (elkhorn
coral) (Goldberg 1973).
Corals are typically exposed during local summer-
time to temperatures near the upper limits of their
thermal tolerances (Hoegh-Guldberg 1999). Although
elevated water temperatures are clearly detrimental to
corals, the response of reef ecosystems to high temper-
ature is less clear. Unlike cold stress, there is little evi-
dence to suggest that maximum temperature currently
limits the latitudinal distribution of coral reefs
(Kleypas in press). Nevertheless, coral reefs are consid-
ered to be the ecosystems most threatened by global
warming (Hoegh-Guldberg 1999; Kleypas et al. 2001;
Walther et al. 2002).
Field and laboratory studies have shown unequivocally
that sustained, anomalously high summertime water tem-
peratures are associated with bleaching (the expulsion of
zooxanthellae by corals and other symbiotic reef organ-
isms; Figure 5). If temperatures rise above the average
maximum for a prolonged period, bleaching leads to death
in many species (Hoegh-Guldberg 1999). Bleaching is not
always fatal, however, and some episodes have been fol-
lowed by recovery of most of the affected coral colonies
(Fitt et al. 1993).
Coral bleaching in response to anomalously high sum-
mer-season temperatures has become more frequent
since the early 1980s (Hoegh-Guldberg 1999). The
widespread nature of these bleaching events over the
past two decades is correlated with increases in maxi-
mum SST (Kleypas et al. 2001). On a global scale, tem-
perature-induced bleaching is usually correlated with
inter-annual climatic fluctuations, of which the El
Niño–Southern Oscillation (ENSO) is the most impor-
tant. During the ENSO-induced global coral bleaching
of 1998, an estimated 16% of the world’s reef-building
corals died (Walther et al. 2002). These bleaching
episodes are dramatic, but they have not been tied to the
extinction of any reef-building species in the Caribbean
or elsewhere. The projected continuing increase in
bleaching episodes on coral reefs, related to ENSO
events and augmented by global warming, is likely to
decrease coral abundance in the future (Hoegh-
Guldberg 1999; Wellington et al. 2001; Aronson et al.
2002; Hughes et al. 2003; Sheppard 2003).
The catastrophic loss of coral cover on Florida’s reefs
over the past 25 years (Shinn 1989; Precht and Miller in
press) could persist for decades or longer. It is unclear
how future global climate change will interact with dis-
ease (Figure 6) and other stresses (Harvell et al. 1999;
Aronson and Precht 2001; Kleypas et al. 2001;
Knowlton 2001; Hughes et al. 2003), but it is known
that the virulence of some coral diseases increases with
rising temperature (Rosenberg and Ben-Haim 2002).
We are faced with two essential questions related to
global temperatures: (1) will the latitudinal ranges of
coral species and coral reefs expand toward the Poles?;
and (2) will corals and coral reefs be eliminated from
low-latitude tropical regions?
309
© The Ecological Society of America www.frontiersinecology.org
Figure 3. Map of Florida showing the present-day distribution
of the reef tract and the northern limit of acroporid corals
(green), the relict Holocene reef tract dominated by acroporid
corals (orange), and the location of recently discovered thickets
of acroporid corals (star).
Figure 4. Patterns of generic diversity of scleractinian corals in
the Caribbean. Rapid faunal diminution along the east coast of
Florida is due to cold temperature limitations. The area in yellow
represents the known distribution of Caribbean acroporids.
Modified from Porter and Tougas (2001).
Global change and coral reefs WF Precht and RB Aronson
The present
Recent studies of marine and coastal systems at middle
and high latitudes have suggested biogeographical shifts,
with increased numbers of warm-water species and
decreased numbers of cold-water species (Weinberg et al.
2002). Few studies have documented such changes in the
tropics, and we know very little about the response of the
extant biota at lower latitudes in the marine realm.
Predicted increases in tropical temperatures (Buddemeier
et al. 2004) will probably have dramatic effects on the
structure and function of these ecosystems and their ser-
vices (Walther et al. 2002), including the introduction,
spread, and dominance of exotic species, and the possible
extinction of native species (McLaughlin et al. 2002;
Stachowicz et al. 2002).
There is mounting evidence that coral species are
responding to recent patterns of increased SSTs by
expanding their latitudinal ranges. One example is the
recent range expansion in the Caribbean and Gulf of
Mexico of Tubastrea coccinea, the first Indo–Pacific coral
species known to have been introduced to the western
Atlantic (Fenner 2001). In Florida, numerous thickets of
staghorn coral, some up to 700 m2in area, are now estab-
lished north of their previously known range. Detailed
studies documenting the composition, structure, and
reproductive viability of these populations have been con-
ducted in seven of these thickets (Vargas-Ángel et al.
2004). Elkhorn coral has also been observed colonizing
shallow reef areas north of extant populations. The two
Acropora species have expanded more than 50 km north-
ward in just the last few decades.
Many factors could be causing the
recent change in distribution of acro-
porid corals, including competition
with macroalgae, changes in habitat
quality, short-term population vari-
ability, indirect interspecific interac-
tions, and variations in reproductive
and recruitment success. Abiotic
parameters influencing their distrib-
ution could include changes in tur-
bidity and water quality, the magni-
tude and frequency of ENSO events,
variations in local and regional
hydro-meteorological forcing pat-
terns, changes in the direction and
intensity of the northward-flowing
Florida Current, and changing pat-
terns in the frequency and duration
of upwelling. Although it is likely
that many of these processes are
occurring and interacting with one
another, the most obvious explana-
tion for the recent range expansion
of acroporids is climatic warming.
We draw this inference based on the
following observations:
(1) The geographic distribution of reef-building corals
along the east coast of Florida is, in general, strongly
correlated with temperature
(2) Acropora spp are temperature-sensitive, and episodes
of mass mortality in Florida have been linked to cold-
water outbreaks
(3) The recent range expansion of the acroporids coin-
cides with a known period of climatic warming and
measured increases in SSTs
(4) The range expansion coincides with a period of ther-
mal stress (bleaching) of reef-building corals world-
wide
(5) The range expansion in Florida coincides with the
discovery of elkhorn coral at the Flower Garden
Banks in the northern Gulf of Mexico
(6) The range expansion coincides with similar range
shifts in Indo-Pacific coral species
(7) The present-day range expansion of western Atlantic
acroporids resembles a change in the geographic distri-
bution of acroporid-dominated reef systems during a
millennial-scale climate flicker thousands of years ago.
The past
Florida’s biogeographic precedent for today’s range
expansion correlates with a period of global warming ear-
lier in the Holocene epoch. This historical example
(Lighty et al. 1978) can be used as an analogue to model
the future response of the Florida reef tract to high-ampli-
tude climate flickers and global warming, even though
310
www.frontiersinecology.org © The Ecological Society of America
Figure 5. Colony of completely bleached elkhorn coral during a severe coral bleaching
event in 1998. Global coral bleaching episodes have been linked to elevated sea surface
temperatures. Photo taken at Looe Key, FL, in August 1998.
WF Precht and RB Aronson Global change and coral reefs
the climatic mechanisms producing the
earlier warm period were different from
those operating at present. SSTs in the
subtropical western Atlantic increased
from 14 000 years before present (ybp)
to the beginning of the Holocene,
about 10 000 ybp; these were higher
than today’s SSTs during the early to
middle Holocene, 10 000 to 6000 ybp;
and declined to modern values in the
late Holocene, 6000 ybp to present
(Balsam 1981; Ruddiman and Mix
1991). This millennial-scale tempera-
ture pattern was probably caused by a
reorganization of North Atlantic circu-
lation similar to Dansgaard-Oeschger
cycles (Kerr 1996). Through the
Quaternary, Dansgaard-Oeschger cycles
have occurred every few thousand years
and have been characterized by abrupt
jumps in temperature.
Relict, submerged, early to middle Holocene reefs are
found throughout southeast Florida (Toscano and
Macintyre 2003; Figure 7). Warmer conditions during this
period apparently permitted a more northerly distribution
of acroporid-dominated reefs (Figure 3). As temperatures
cooled after the middle Holocene, the northern limit of
the Florida reef tract moved south to its current position.
In the early to middle Holocene, Acropora-dominated
reefs up to 10 m thick were well developed as far north as
Palm Beach County (Lighty et al. 1978), indicating that
conditions along the platform margin were more con-
ducive than today to the growth of acroporid corals and
the deposition of acroporid-dominated
reef framework (Figure 8). We inter-
pret the more northerly distribution of
Acropora as a reflection of northward
excursions of warm water related to a
unique conjunction of factors. First,
lower sea levels during this time placed
the active shelf-margin reef system in
closer proximity to the warmer waters
of the Florida Current. Second, the
period from about 9000–5000 ybp
corresponds to the warmest interval of
the Holocene, the Mid-Holocene
Warm (Kerwin et al. 1999) or
Altithermal (Buddemeier et al. 2004).
Although tropical temperatures
remained relatively stable through the
middle Holocene, within 1.0–1.5°C of
present values (Arz et al. 2001), paleo-
temperatures reconstructed from the
extratropical North Atlantic indicate
SSTs 2–3°C warmer than at present
(Balsam 1981; Ruddiman and Mix
1991). Climate simulations suggest
that North Atlantic SSTs at 6000 ybp were as much as
4°C warmer than today (Kerwin et al. 1999). Evidence
from both terrestrial and coastal habitats shows that
warming during this millennial-scale, high-amplitude cli-
mate flicker caused many species from a variety of ecosys-
tems to expand their ranges northwards (COHMAP
1988; Delcourt and Delcourt 1991; Dahlgren et al. 2000).
The climate flicker during the middle Holocene also
correlates with maximal coral diversity at the northern-
most position of coral reefs in the Pacific. The world’s
highest latitude Pacific coral reef is currently in Tateyama,
Japan (33.5°N). Veron’s (1992) study of a mid-Holocene
311
© The Ecological Society of America www.frontiersinecology.org
Figure 7. Idealized cross-section showing three shore-parallel relict reef ridges off
Broward County, FL. The lower ridge was described by Lighty et al. (1978) at
Hillsborough Inlet and the middle ridge by Precht et al. (2000) at Dania Beach.
Radiocarbon dates of recovered elkhorn coral revealed substantial early- to middle-
Holocene reef development off the east coast of Florida, extending north to Palm Beach
County. Figure modified from originals in Lighty et al. (1978) and Toscano and
Macintyre (2003).
Figure 6. White-band disease and resultant “branch-to-tip” mortality pattern
observed on a colony of elkhorn coral at Carysfort Reef, FL. Photo taken in 1999.
Global change and coral reefs WF Precht and RB Aronson
fossil reef at Tateyama showed that even a brief period of
warming of only 2°C doubled species richness from 35 to
72 species at the latitudinal extreme of extant corals. At
the southernmost living reef in the Pacific Ocean, Lord
Howe Island in Australia (31.3°S), evidence indicates
that reefs were better developed in the early to middle
Holocene than today, suggesting similar responses of
corals to fluctuating SSTs.
Another paleoecological example is found in the
Pleistocene reef community at Rottnest Island off
Western Australia (32°S). The living reef at this locality
has some 25 species of zooxanthellate corals. Most are at
the southern limit of their range, with Acropora spp being
rare (Marsh 1992); however, during the last major inter-
glacial (about 125 000 ybp), when the water was a few
degrees warmer, major reefs were formed by both staghorn
and tabular Acropora spp (Szabo 1979). These paleoeco-
logical examples of species replacements and range expan-
sions, especially those concerning acroporids, emphasize
the varied responses of coral species and their ability to
reconstitute reef communities in the face of rapid environ-
mental change not related to human modification of the
seascape. Understanding the response of reef organisms to
warm climates of the past, regardless of the underlying
causes, will help us predict the future of coral reefs in a
warming world.
The future
The modeled range of global temperature increase is
1.4–5.8°C for the period 1990–2100 (Buddemeier et al.
2004). However, these models predict an SST warming of
only 1–3°C in the tropics during the same period.
Relative conservatism of tropical temperatures and
greater warming of extratropical areas are likely to result
from feedbacks in the ocean–atmos-
phere system, which prevents SSTs
from exceeding 32°C (Kleypas in
press). General circulation models
indicate that tropical heating, espe-
cially near the equator, increases latent
heat flux away from the tropics. The
predicted difference in temperature
rise between the tropics and extratrop-
ical areas is remarkably similar to those
recorded through the glacial–inter-
glacial cycles of the Quaternary Period
(the last 1.8 million years; CLIMAP
1984).
The National Research Council
(1988) recommended that studies doc-
umenting population, community, and
ecosystem responses to rapid environ-
mental changes of the Quaternary be
used to provide insight into the rates
and directions of future biotic change.
Specifically, such paleoecologic studies
allow us to evaluate biotic response to environmental
changes of magnitudes that are beyond recent values but
within the range of projected global change. Although
fossil assemblages from a number of ecosystems have no
analogues in modern communities (Roy et al. 1996), mod-
ern reef communities closely resemble fossil reef assem-
blages (Pandolfi and Jackson 1997).
It has been argued that tropical coral assemblages
exhibit stability and persistence through Quaternary time
and therefore constitute the most important database for
studying abrupt change in modern reefs (Pandolfi and
Jackson 1997). A key aspect of this argument is that
warmer temperatures during the last major interglacial
period were not associated with contraction of the south-
ern range of the acroporids or the demise of reef systems in
the tropics. Based on these results, and because SSTs in
global climate models generally do not exceed 32°C in the
Caribbean, it is unlikely that future global warming will
lead to the catastrophic collapse of reef systems, the extir-
pation of acroporid corals, or the contraction of their
southern range in the tropical Caribbean, as some have
predicted (eg Hoegh-Guldberg 1999; Reaser et al. 2000).
Reefs living under non-optimal conditions in more ther-
mally reactive areas, including those in Florida, the Gulf
of Mexico, and Bermuda, are more likely to show changes
in species richness and diversity with climatic warming
(Precht and Miller in press).
At the latitudinal extremes of Caribbean reef systems,
an increase in SST of only 1–2°C should encourage tem-
perature-sensitive corals such as the acroporids to expand
their ranges. Reyes Bonilla and Cruz Piñón (2002) made a
similar prediction for warming seas along the Pacific coast
of Mexico, suggesting that coral species richness will
increase the most at subtropical latitudes. Along the east-
ern Pacific, as many as eight coral species have recently
312
www.frontiersinecology.org © The Ecological Society of America
Figure 8. Underwater photograph of excavated in situ colony of elkhorn coral from a
Holocene-age relict reef off Ft Lauderdale, FL. Colony in photo was radiocarbon-
dated to 6980 calendar years before present.
WF Precht and RB Aronson Global change and coral reefs
been identified north of their previously known ranges
(H Reyes Bonilla pers comm), while at Lord Howe
Island in Australia the arrival of six species has been
observed within the past decade (JEN Veron pers
comm). In addition to temperature, however, other fac-
tors including light, carbonate saturation state, pollu-
tion, and disease influence reef development
(Buddemeier et al. 2004). Increases in extreme weather
and climate events will also probably occur in the
future, especially at middle to high latitudes (Easterling
et al. 2000). Associated habitat loss due to these multi-
ple stressors will further complicate our ability to pro-
ject geographic distributions of species and communi-
ties under future climates (Pyke 2004). We cannot
predict how these controls will interact, meaning that
further climate change could cause the latitudinal
ranges of coral reefs to expand, remain stable, or even
contract (Kleypas in press). Furthermore, the north-
ward expansion of Caribbean reefs will be limited by
the shift from a carbonate-dominated to a siliciclastic-
dominated sedimentary regime, as well as by increasing
nutrient concentrations, as one moves north along the
east coast of the Florida Peninsula, further confounding
future predictions.
The staghorn coral thickets off Fort Lauderdale present
an interesting case. Are these remnant populations, or are
they the recent product of a chance recruitment event?
Do they represent a temporary range expansion that is
likely to be obliterated by the passage of the next sub-
freezing cold front, disease outbreak, or hurricane? Are
they an indicator of global climate change? These possibil-
ities are not mutually exclusive, but only through genetic
analysis of populations and long-term monitoring will we
be able to answer such questions definitively.
The fossil record of coral reefs is helping us predict the
impacts of future climatic warming. Although it is likely
that reef-building corals will expand their ranges to higher
latitudes in response to global warming, geographic shifts
of marginal reefs will not mitigate the expected ecological
and economic losses due to localized coral mortality and
reduced function in tropical reef systems. Understanding
the causal links between climate change and the dynamics
of reefs and other ecosystems will continue to be a chal-
lenge in the face of natural variability, uncertainties inher-
ent in predictive models, and the complex impacts of
human activity all over the planet.
Acknowledgements
We thank Dick Dodge, Peter Glynn, Joanie Kleypas, Ian
Macintyre, Steven Miller, Hector Reyes Bonilla,
Bernhard Riegl, Martha Robbart, James Thomas, Maggie
Toscano, Bernardo Vargas-Ángel, and Charlie Veron for
advice and discussion. Ian Macintyre provided funds for
radiocarbon dating the samples described in Figure 6.
Beta Analytic, Inc. of Miami performed the 14C dating.
Sarah Bernhardt discovered Acropora palmata at the
Flower Garden Banks in the northwestern Gulf of
Mexico. Funding for this work was provided by the US
Department of the Interior’s Minerals Management
Service (contract GM-02-04 to WFP) and the US
National Science Foundation (grant EAR-9902192 to
RBA). This is Contribution No. 355 from the Dauphin
Island Sea Lab.
References
Aronson RB and Precht WF. 2001. White-band disease and the
changing face of Caribbean coral reefs. Hydrobiologia 460:
25–38.
Aronson RB, Precht WF, Toscano MA, and Koltes KH. 2002. The
1998 bleaching event and its aftermath on a coral reef in
Belize. Mar Biol 141: 435–47.
Arz HW, Gerhardt S, Pätzold J, and Röhl U. 2001. Millennial-scale
changes of surface- and deep-water flow in the western tropical
Atlantic linked to Northern Hemisphere high-latitude climate
during the Holocene. Geology 29: 239–42.
Balsam W. 1981. Late Quaternary sedimentation in the western
North Atlantic: stratigraphy and paleoceanography.
Palaeogeogr Palaeoclimatol Palaeoecol 35: 215–40.
Barnett TP, Pierce DW, and Schnur R. 2001. Detection of anthro-
pogenic climate change in the world’s oceans. Science 292:
270–74.
Buddemeier RW, Kleypas JA, and Aronson RB. 2004. Coral reefs
and global climate change: potential contributions of climate
change to stresses on coral reef ecosystems. Arlington,VA: Pew
Center on Global Climate Change.
CLIMAP Project Members. 1984. The last interglacial ocean. Quat
Res 21: 123–224.
COHMAP Members. 1988. Climatic changes of the last 18,000
years: observations and model simulations. Science 241:
1043–52.
Dahlgren TG, Weinberg JR, and Halanych KM. 2000.
Phylogeography of the ocean quahog (Artica islandica): influ-
ences of paleoclimate on genetic diversity and species range.
Mar Biol 137: 487–95.
Delcourt HR and Delcourt PA. 1991. Quaternary ecology – a pale-
oecological perspective. London, UK: Chapman and Hall.
Easterling DR, Meehl GA, Parmesan C, et al. 2000. Climate
extremes: observations, modeling, and impacts. Science 289:
2068–74.
Fenner D. 2001. Biogeography of three Caribbean corals
(Scleractinia) and the invasion of Tubastraea coccinea into the
Gulf of Mexico. Bull Mar Sci 69: 1175–89.
Fields PA, Graham JB, Rosenblatt RH, and Somero GN. 1993.
Effects of expected global climate change on marine faunas.
Trends Ecol Evol 8: 361–67
Fitt WK, Spero HJ, Halas J, et al. 1993. Recovery of the coral
Montastrea annularis in the Florida Keys after the 1987
Caribbean “bleaching event”. Coral Reefs 12: 57–64.
Gardner TA, Côté IM, Gill JA, et al. 2003. Long-term region-wide
declines in Caribbean corals. Science 301: 958–60.
Goldberg WM. 1973. The ecology of the coral–octocoral commu-
nities off the southeast Florida coast: geomorphology, species
composition, and zonation. Bull Mar Sci 23: 465–87.
Graus RR and Macintyre IG. 1998. Global warming and the future
of Caribbean coral reefs. Carb Evap 13: 43–47.
Harvell CD, Kim K, Burkholder JM, et al. 1999. Emerging marine
diseases – climate links and anthropogenic factors. Science 285:
1505–10.
Hoegh-Guldberg O. 1999. Climate change, coral bleaching and
the future of the world’s coral reefs. Mar Freshwat Res 50:
839–66.
Hughes TP, Baird AH, Bellwood DR, et al. 2003. Climate change,
313
© The Ecological Society of America www.frontiersinecology.org
Global change and coral reefs WF Precht and RB Aronson
human impacts, and the resilience of coral reefs. Science 301:
929–33.
Kerr RA. 1996. Millennial climate oscillation spied. Science 271:
146–47.
Kerwin M, Overpeck JT, Webb RS, et al. 1999. The role of oceanic
forcing in mid-Holocene Northern Hemisphere climatic
change. Paleoceanography 14: 200–10.
Kleypas JA. Constraints on predicting coral reef response to cli-
mate change. In: Aronson RB (Ed). Geological approaches to
coral reef ecology. New York: Springer-Verlag. In press.
Kleypas JA, Buddemeier RW, and Gattuso J-P. 2001. The future of
coral reefs in an age of global change. Geol Rundsch 90:
426–37.
Knowlton N. 2001. The future of coral reefs. Proc Natl Acad Sci
USA 98: 5419–25.
Levitus S, Antonov JI, Boyer TP, and Stephens C. 2000. Warming
of the world ocean. Science 287: 2225–28.
Lighty RG, Macintyre IG, and Stuckenrath R. 1978. Submerged
early Holocene barrier reef south-east Florida shelf. Nature
276: 59–60.
Marsh LM. 1992. The occurrence and growth of Acropora in extra-
tropical waters off Perth, Western Australia. Guam: Proc 7th
Intl Coral Reef Symp 2: 1233–38.
McLaughlin JF, Hellmann JJ, Boggs CL, and Ehrlich PR. 2002.
Climate change hastens population extinctions. Proc Natl Acad
Sci USA 99: 6070–74.
National Research Council. 1988. Toward an understanding of
global change. Washington, DC: National Academy Press.
Pandolfi JM and Jackson JBC. 1997. The maintenance of diversity
on coral reefs: examples from the fossil record. Panama: Proc
8th Intl Coral Reef Symp 1: 397–404.
Parmesan C and Yohe G. 2003. A globally coherent fingerprint of
climate change impacts across natural systems. Nature 421:
37–42.
Porter JW and Tougas JI. 2001. Reef ecosystems: threats to their
biodiversity. In: Encyclopedia of biodiversity. New York:
Academic Press 5: 73–95.
Precht WF, Macintyre IG, Dodge RE, et al. 2000. Backstepping of
Holocene reefs along Florida’s east coast. Bali: Abstracts 9th Intl
Coral Reef Symp. p 321.
Precht WF and Miller SL. Ecological shifts along the Florida reef
tract: the past as a key to the future. In: Aronson RB (Ed).
Geological approaches to coral reef ecology. New York:
Springer-Verlag. In press.
Pyke CR. 2004. Habitat loss confounds climate change impacts.
Front Ecol Environ 2: 178–82.
Reaser JK, Pomerance R, and Thomas PO. 2000. Coral bleaching
and global climate change: scientific findings and policy rec-
ommendations. Conserv Biol 14: 1500–11.
Reyes Bonilla H and Cruz Piñón G. 2002. Influence of temperature
and nutrients on species richness of deep-water corals from the
western coast of the Americas. Hydrobiologia 471: 35–41.
Root TL, Price JT, Hall KR, et al. 2003. Fingerprints of global
warming on wild animals and plants. Nature 421: 57–60.
Rosenberg E and Ben-Haim Y. 2002. Microbial diseases of corals
and global warming. Env Microbiol 4: 318–26.
Roy K, Valentine JW, Jablonski D, and Kidwell SM. 1996. Scales of
climatic variability and time averaging in Pleistocene biotas:
implications for ecology and evolution. Trends Ecol Evol 11:
458–63.
Ruddiman WF and Mix AC. 1991. The north and equatorial
Atlantic at 9000 and 6000 yr B.P. In: HE Wright Jr, JE
Kutzbach, T Webb III, et al. (Eds). Global climates since the
last glacial maximum. Minneapolis: University of Minnesota
Press. p 94–124.
Sheppard CRC. 2003. Predicted recurrences of mass coral mortal-
ity in the Indian Ocean. Nature 425: 294–97.
Shinn EA. 1989. What is really killing the corals? Sea Frontiers 35:
72–81.
Shinn EA, Lidz BH, Kindinger JL, Hudson JH, and Halley RB.
1989. Reefs of Florida and the Dry Tortugas. Field Trip
Guidebook T176. Washington, DC: American Geophysical
Union.
Stachowicz JL, Terwin JR, Whitlatch RB, and Osman RW. 2002.
Linking climate change and biological invasions: ocean warm-
ing facilitates nonindigenous species invasions. Proc Natl Acad
Sci USA 99: 15497–500.
Szabo BJ. 1979. Uranium-series age of coral reef growth on
Rottnest Island, Western Australia. Mar Geol 29: M11–M15.
Toscano MA and Macintyre IG. 2003. Corrected western Atlantic
sea-level curve for the last 11,000 years based on calibrated 14C
dates from Acropora palmata and mangrove intertidal peat.
Coral Reefs 22: 257–70.
Vargas-Ángel B, Thomas JD, and Hoke SM. 2003. High-latitude
Acropora cervicornis thickets off Fort Lauderdale, Florida, USA.
Coral Reefs 22: 465–74.
Veron JEN. 1992. Environmental control of Holocene changes to
the world’s most northern hermatypic coral outcrop. Pac Sci 46:
405–25.
Walther G-R, Post E, Convey P, et al. 2002. Ecological responses to
recent climate change. Nature 416: 389–95.
Weinberg JR, Dahlgren TG, and Halanych KM. 2002. Influence of
rising sea temperature on commercial bivalve species of the U.
S. Atlantic coast. Amer Fish Soc Symp 32: 131–40.
Wellington GM, Glynn PW, Strong AE, et al. 2001. Crisis on coral
reefs linked to climate change. Eos 82: 1,5.
314
www.frontiersinecology.org © The Ecological Society of America
