www.sciencemag.org SCIENCE VOL 307 18 MARCH 2005
oral reefs provide ecosys-
tem goods and services
worth more than $375 bil-
lion to the global economy each
year (1). Yet, worldwide, reefs are
in decline (1–4). Examination of
the history of degradation reveals
three ways to challenge the cur-
rent state of affairs (5, 6). First,
scientists should stop arguing
about the relative importance of
different causes of coral reef decline: overfish-
ing, pollution, disease, and climate change.
Instead, we must simultaneously reduce all
threats to have any hope of reversing the
decline. Second, the
scale of coral reef
mechanisms such as
has been too small and piecemeal. Reefs must
be managed as entire ecosystems. Third, a lack
of clear conservation goals has limited our
ability to define or measure success.
Large animals, like turtles, sharks, and
groupers, were once abundant on all coral
reefs, and large, long-lived corals created a
complex architecture supporting diverse
fish and invertebrates (5, 6). Today, the most
degraded reefs are little more than rubble,
seaweed, and slime. Almost no large ani-
mals survive, water quality is poor, and
large corals are dead or dying and being
replaced by weedy corals, soft corals, and
seaweed (2, 7, 8). Overfishing of megafauna
releases population control of smaller fishes
and invertebrates, creating booms and busts.
This in turn can increase algal overgrowth,
or overgrazing, and stress the coral archi-
tects, likely making them more vulnerable
to other forms of stress. This linked
sequence of events is remarkably consistent
worldwide (see top figure, this page).
Even on Australia’s Great Barrier Reef
(GBR), the largest and best-managed reef in
the world, decline is ongoing (9). Australia’s
strategy, beginning with the vision to estab-
lish the world’s largest marine park in 1976,
is based on coordinated
management at large
spatial scales. Recently
more than one-third of
the GBR was zoned
“no take,” and new
laws and policies to
reduce pollution and
fishing are in place
(10). Evaluating bene-
fits of increased no-
take zones will require
detailed follow-up, but
elsewhere support in-
creased protection. Two
the Bahamas (11) and
Cuba (12), have also
committed to conserve
more than 20% of their
coral reef ecosystems.
By contrast, the Florida
Keys and main Ha-
waiian Islands are far
further down the trajec-
tory of decline (see bottom figure, this
page), yet much less action has been taken.
What is the United States doing to
enhance its coral reef assets? In the Florida
Keys National Marine Sanctuary, the
Governor and the National Oceanic and
Atmospheric Administration (NOAA)
agreed in 1997 to incorporate zoning with
protection from fishing and water quality
controls (13). But only 6% of
the Sanctuary is zoned no take,
and these zones are not strategi-
cally located. Conversion of
16,000 cesspools to centralized
sewage treatment and control of
other land-based pollution have
only just begun. Florida’s reefs
are well over halfway toward
ecological extinction and much
more impaired than reefs of
Belize and all but one of the
Pacific reefs in the figure below (6). Large
predatory fishes continue to decrease (14),
reefs are increasingly dominated by seaweed
(15, 16), and alarming diseases have
Annual revenues from reef tourism are
$1.6 billion (1), but the economic future of the
Keys is gloomy owing to accelerating ecolog-
ical degradation. Why? Without a clear goal
for recovery, development and ratification of
the management plan became a goal in itself.
Reefs of the northwest Hawaiian Islands
have been partially protected by isolation from
the main Hawaiian Islands (which show
Are U.S. Coral Reefs on
the Slippery Slope to Slime?
J. M. Pandolfi,
* J. B. C. Jackson,
R. H. Bradbury,
H. M. Guzman,
T. P. Hughes,
J. C. Ogden,
H. P. Possingham,
CREDIT: (TOP) MARY PARRISH
The slippery slope of coral reef decline through time.
1500 1600 1700 1800 1900 2000 2100
Main Hawaiian Islands,
NW Hawaiian Islands,
Jamaica, W Panamá
Bahamas, E Panamá
Belize, N Red Sea
S Red Sea
Past and present ecosystem conditions of 17 coral reefs,based on his-
torical ecology (
). The method consists of determining the status of
guilds of organisms for each reef with published data, performing a multi-
variate, indirect gradient analysis on the guild status database, and esti-
mating the location of each reef along a gradient of degradation from pris-
tine to ecologically extinct reefs. Green, Caribbean sites; blue,Australian
and Red Sea sites; red, U.S. reefs from the most recent cultural period.
The Centre for Marine Studies and Department of
Department of Mathematics and
School of Life Sciences,The University of Queensland,
St. Lucia, QLD 4072, Australia.
Center for Marine
Biodiversity and Conservation, Scripps Institution of
Oceanography, La Jolla, CA 92093, USA.
Tropical Research Institute, Balboa, Republic of
National Center for Ecological Analysis and
Synthesis, Santa Barbara CA.
Centre for Resource and
Environmental Studies, Australian National
University, Canberra, ACT 0200, Australia.
Coral Reef Biodiversity, School of Marine Biology,
James Cook University, Townsville, QLD 4811,
Hopkins Marine Station, Stanford
University, CA 93950–3094, USA.
Florida Institute of
Oceanography, St. Petersburg, FL 33701, USA.
*Author for correspondence. E-mail: j.pandolfi@
Enhanced online at
Published by AAAS
on November 12, 2010 www.sciencemag.orgDownloaded from
CORRECTED 17 JUNE 2005; SEE LAST PAGE
degradation similar to that of the Florida Keys)
and are in relatively good condition (see figure
at the bottom of page 1725). Corals are healthy
(2, 18), and the average biomass of commer-
cially important large predators such as sharks,
jacks, and groupers is 65 times as great (19) as
that at Oahu, Hawaii, Maui, and Kauai. Even in
the northwestern islands, however, there are
signs of decline. Monk seals and green turtles
are endangered (20, 21); large amounts of
marine debris are accumulating, which injure
or kill corals, seabirds, mammals, turtles, and
fishes (2, 18, 22); and levels of contaminants,
including lead and PCBs are high (18).
Until recently, small-scale impacts from
overfishing and pollution could be managed
locally, but thermal stress and coral bleach-
ing are already changing community struc-
ture of reefs. Impacts of climate change may
depend critically on the extent to which a
reef is already degraded (8, 23). Polluted and
overfished reefs like in Jamaica and Florida
have failed to recover from bouts of bleach-
ing, and their corals have been replaced by
seaweed (2). We believe that restoring food
webs and controlling eutrophication pro-
vides a first line of defense against climate
change (8, 23); however, slowing or revers-
ing global warming trends is essential for the
long-term health of all tropical coral reefs.
For too long, single actions such as mak-
ing a plan, reducing fishing or pollution, or
conserving a part of the system were viewed
as goals. But only combined actions
addressing all these threats will achieve the
ultimate goal of reversing the trajectory of
decline (see the table above).
We need to act now to curtail processes
adversely affecting reefs. Stopping overfish-
ing will require integrated systems of no-
take areas and quotas to restore key func-
tional groups. Terrestrial runoff of nutrients,
sediments, and toxins must be greatly
reduced by wiser land use and coastal devel-
opment. Reduction of emissions of green-
house gases are needed to reduce coral
bleaching and disease. Progress on all fronts
can be measured by comparison with the
past ecosystem state through the methods of
historical ecology to determine whether or
not we are succeeding in ameliorating or
reversing decline. Sequential return of key
groups, such as parrot fish and sea urchins
that graze down seaweed; mature stands of
corals that create forest-like complexity; and
sharks, turtles, large jacks, and groupers that
maintain a more stable food web (4, 5, 6, 24)
This consistent way of measuring recov-
ery (see the figure at the bottom of page
1725) and the possibility of short-term
gains set a benchmark for managing other
marine ecosystems. Like any other success-
ful business, managing coral reefs requires
investment in infrastructure. Hence, we also
need more strategic interventions to restore
species that provide key ecological func-
tions. For example, green turtles and sea
cows not only once helped maintain healthy
seagrass ecosystems, but also were an
important source of high-quality protein for
coastal communities (25).
Our vision of how to reverse the decline
of U.S. reefs rests on addressing all threats
simultaneously (see the table above). By
active investment, major changes can be
achieved through practical solutions with
short- and long-term benefits. Short-lived
species, like lobster, conch, and aquarium
fish will recover and generate income in just
a few years, and benefits will continue to
compound over time. Longer-lived species
will recover, water quality will improve, and
the ecosystem will be more resilient to
unforeseen future threats. Ultimately, we will
have increased tourism, and the possibility of
renewed sustainable extraction of abundant
megafauna. One day, reefs of the United
States could be the pride of the nation.
Reefs at Risk. A Map-Based Indicator of
Threats to the World’s Coral Reefs
Institute,Washington, DC, 1998).
2. C. R.Wilkinson,
Status of Coral Reefs of the World:
(Global Coral Reef Monitoring Network and
Australian Institute of Marine Science, Townsville,
Australia, in press); vol. 1 is available at
3. T.A. Gardener
301, 958 (2003).
4. D. R. Bellwood, T. P. Hughes, C. Folke, M. Nyström,
429, 827 (2004).
5. J. B. C. Jackson
293, 629 (2001).
6. J. M. Pandolfi
301, 955 (2003).
7. T. P. Hughes
265, 1547 (1994).
8. N. Knowlton,
Proc. Natl. Acad. Sci. U.S.A.
9. Great Barrier Reef Marine Park Authority,
The current status of the Great Barrier Reef
10. Great Barrier Reef Marine Park Authority, New Policy
Web site: www.gbrmpa.gov.au/corp_site/manage-
11. D. R. Brumbaugh
Proceedings of the Forum 2003
, Nassau, Bahamas, 30 June to 4 July 2003
(College of the Bahamas, Nassau, Bahamas, 2003).
12. R. Estrada
El sistema nacional de areas marinas
protegidas de Cuba
[Center for Protected Areas
(CNAP), Havana, Cuba, 2003].
13. Florida Keys National Marine Sanctuary,
Management Plan/Environmental Impact Statement
(Department of Commerce, National Oceanic and
Atmospheric Administration,Washington, DC, 1995),
vol. 1, pp.1–323.
14. J.A. Bohnsack,
Gulf Caribbean Res.
14, 1 (2003).
15. W. C. Jaap
Environmental Protection Agency/
National Oceanographic and Atmospheric
Administration (NOAA) Coral Reef Evaluation and
Monitoring Project: 2002 Executive Summary
of the Florida Fish and Wildlife Conservation
Commission, Tallahassee, and the University of
16. J.W. Porter
The Everglades, Florida Bay, and
Coral Reefs of the Florida Keys: An Ecosystem
, J.W. Porter and K. G. Porter, Eds. (CRC Press,
Boca Raton, FL, 2002), pp. 749–769.
17. C. D. Harvell
296, 2158 (2002).
18. J. Maragos, D. Gulko, Eds.,
Coral Reef Ecosystems of the
Northwestern Hawaiian Islands: Interim Results
Emphasizing the 2000 Surveys
(U.S. Fish and Wildlife
Service and Hawaii Department of Land and Natural
Resources, Honolulu, HI, 2002).
19. A. M. Friedlander, E. E. DeMartini,
Mar. Ecol. Prog. Ser.
230, 253 (2002).
20. International Union for the Conservation of Nature
and Natural Resources,
Red List of Threatened Species
available at www.redlist.org.
21. NOAA, www.nmfs.noaa.gov/prot_res/species/.
22. C. Safina,
Eye of the Albatross
(Holt, New York, 2003).
23. T. P. Hughes
301, 929 (2003).
24. T. Elmqvist
Front. Ecol. Environ.
1, 488 (2003).
25. J. B. C. Jackson,
16, S23 (1997).
Supporting Online Material
A ROADMAP FOR REVERSING THE TRAJECTORY OF DECLINE OF U.S. CORAL REEFS
Threat (time frame) Critical first step Results Benefits
Overfishing Immediate increase of cumulative Increase in short-lived species, Economic viability to lost or
(years) no-take areas of all U.S. reefs to >30%; such as lobsters, conch, weakened fisheries; reduction in
reduce fishing efforts in adjacent areas parrotfish, and sea urchins algal competition with corals
Overfishing Establishment of large fish, shark, turtle, Increase in megafauna Return of key functional
(decades) and manatee breeding programs; populations components and trophic structure
mandatory turtle exclusion devices (TEDs)
and bycatch reduction devices (BRDs)
Pollution Stringent controls over land-based Increase in water quality Reduction in algal competition
(years-decades) pollution with corals; reduced coral disease
Coastal development Moratorium on coastal development Increase in coral reef habitat Increase of coral reef populations
(years-decades) in proximity to coral reefs (i.e., reduced mortality)
Global change International engagement in Reduction in global sea surface Lower incidence of coral bleaching;
(decades) emission caps temperatures and CO
increase calcification potential
18 MARCH 2005 VOL 307 SCIENCE www.sciencemag.org
P OLICY FORUM
Published by AAAS
on November 12, 2010 www.sciencemag.orgDownloaded from
www.sciencemag.org SCIENCE Erratum post date 17 JUNE 2005
Post date 17 June 2005
C ORRECTIONS AND C LARIFICATIONS
Policy Forum: “Are U.S. coral reefs on the slippery slope to slime?” by J. M.
(18 Mar. 2005, p. 1725). In the bottom figure on p. 1725,
Caribbean sites are purple (not green as described in the legend), and some
data points are not seen because of superimposed dots. Otherwise, the labels
point to the dots in order. For example, the Bahamas and eastern Panamá are
represented by the purple dot partly showing above the red dot for the Main
Hawaiian islands and Florida Keys. The lettering for the Outer Great Barrier
Reef (Outer GBR) should be black.
on November 12, 2010 www.sciencemag.orgDownloaded from