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Abstract

Conservation of U.S. coral reefs has been sidetracked by the partial implementation of management plans without clearly achievable goals. Historical ecology reveals global patterns of coral reef degradation that provide a framework for reversing reef decline with ecologically meaningful metrics for success. The authors of this Policy Forum urge action now to address multiple threats simultaneously, because the harmful effects of stressors like overfishing, pollution, poor land-use practices, and global warming are interdependent. Prompt implementation of proven, practical solutions would lead to both short- and long-term benefits, including the return of keystone species and the economic benefits they entail.
www.sciencemag.org SCIENCE VOL 307 18 MARCH 2005
1725
C
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 (14). 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
management—with
mechanisms such as
protected areas—
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
smaller-scale studies
elsewhere support in-
creased protection. Two
neighboring countries,
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
emerged (17).
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
ECOLOGY
Are U.S. Coral Reefs on
the Slippery Slope to Slime?
J. M. Pandolfi,
1
* J. B. C. Jackson,
3,4
N. Baron,
5
R. H. Bradbury,
6
H. M. Guzman,
4
T. P. Hughes,
7
C.V. Kappel,
8
F. Micheli,
8
J. C. Ogden,
9
H. P. Possingham,
2
E. Sala
3
POLICY FORUM
CREDIT: (TOP) MARY PARRISH
?
?
?
R
e
c
o
v
e
r
y
D
e
g
r
a
d
a
t
i
o
n
The slippery slope of coral reef decline through time.
1500 1600 1700 1800 1900 2000 2100
Calenda
r y
ear
Percent degradation
Main Hawaiian Islands,
Florida Keys
NW Hawaiian Islands,
Outer GBR
Virgin Islands,
Moreton Bay
Jamaica, W Panamá
Bahamas, E Panamá
Cayman Islands,
Bermuda
Belize, N Red Sea
S Red Sea
Torres Strait
Inner GBR
0
20
40
60
80
100
Agricultural
Colonial
occupation
Colonial
development
Early
modern
Late
modern
The
future
Past and present ecosystem conditions of 17 coral reefs,based on his-
torical ecology (
6
). 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.
1
The Centre for Marine Studies and Department of
Earth Sciences,
2
Department of Mathematics and
School of Life Sciences,The University of Queensland,
St. Lucia, QLD 4072, Australia.
3
Center for Marine
Biodiversity and Conservation, Scripps Institution of
Oceanography, La Jolla, CA 92093, USA.
4
Smithsonian
Tropical Research Institute, Balboa, Republic of
Panamá.
5
National Center for Ecological Analysis and
Synthesis, Santa Barbara CA.
6
Centre for Resource and
Environmental Studies, Australian National
University, Canberra, ACT 0200, Australia.
7
Centre for
Coral Reef Biodiversity, School of Marine Biology,
James Cook University, Townsville, QLD 4811,
Australia.
8
Hopkins Marine Station, Stanford
University, CA 93950–3094, USA.
9
Florida Institute of
Oceanography, St. Petersburg, FL 33701, USA.
*Author for correspondence. E-mail: j.pandolfi@
uq.edu.au
Enhanced online at
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content/full/307/5716/1725
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CORRECTED 17 JUNE 2005; SEE LAST PAGE
1726
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)
constitutes success.
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.
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Supporting Online Material
www.sciencemag.org/cgi/content/full/307/5716/1725/DC1
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
2
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
1
www.sciencemag.org SCIENCE Erratum post date 17 JUNE 2005
Post date 17 June 2005
ERRATUM
C ORRECTIONS AND C LARIFICATIONS
Policy Forum: “Are U.S. coral reefs on the slippery slope to slime?” by J. M.
Pandolfi
et al.
(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
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... In the last five decades, significant disturbances such as thermal stress, diseases, storms, and pollution have occurred more frequently and with higher intensity, disrupting and eliminating much recovery in the ecological successional process, creating a shifting baseline for "natural" conditions (Alvarez-Filip et al. 2009;Jackson et al. 2011). Community changes in coral species can be subtle because coral species identification is challenging and substantial community changes may occur over decadal, centennial, or millennial timescales (Pandolfi et al. 2005;van Woesik et al. 2012). The potentially slow shift in coral composition emphasizes the importance of establishing and documenting natural reef conditions to help guide and define coral reef conservation and restoration goals, as documented for BCG level 1. ...
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Environmental change is multidimensional, with local anthropogenic stressors and global climate change interacting to differentially impact populations throughout a species’ geographic range. Within species, the spatial distribution of phenotypic variation and its causes (i.e. local adaptation or plasticity) will determine species’ adaptive capacity to respond to a changing environment. However, comparatively little is known about the spatial scale of adaptive differentiation among populations and how patterns of local adaptation might drive vulnerability to global change stressors. To test whether fine-scale (2 - 12 km) mosaics of environmental stress can cause adaptive differentiation in a marine foundation species, eelgrass (Zostera marina), we conducted a three-way reciprocal transplant experiment spanning the length of Tomales Bay, CA. Our results revealed strong home-site advantage in growth and survival for all three populations. In subsequent common garden experiments and feeding assays we show that counter-gradients in temperature, light availability, and grazing pressure from an introduced herbivore contribute to differential performance among populations consistent with local adaptation. Our findings highlight how local-scale mosaics in environmental stressors can increase phenotypic variation among neighboring populations, potentially increasing species resilience to future global change. More specifically, we identified a range-center eelgrass population that is pre-adapted to extremely warm temperatures similar to those experienced by low-latitude range-edge populations of eelgrass, demonstrating how reservoirs of heat-tolerant phenotypes may already exist throughout a species range. Future work on predicting species resilience to global change should incorporate potential buffering effects of local-scale population differentiation and promote a phenotypic management approach to species conservation.
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Ocean warming, fueled by climate change, is the primary cause of coral bleaching events which are predicted to increase in frequency. Bleaching is generally damaging to coral reproduction, can be exacerbated by concomitant stressors like ultraviolet radiation (UVR), and can have lasting impacts to successful reproduction and potential adaptation. We compared morphological and physiological reproductive metrics (e.g., sperm motility, mitochondrial membrane integrity, egg volume, gametes per bundle, and fertilization and settlement success) of two Hawaiian Montipora corals after consecutive bleaching events in 2014 and 2015. Between the species, sperm motility and mitochondrial membrane potential had the most disparate results. Percent sperm motility in M. capitata , which declined to ~ 40% during bleaching from a normal range of 70–90%, was still less than 50% motile in 2017 and 2018 and had not fully recovered in 2019 (63% motile). By contrast, percent sperm motility in Montipora spp . was 86% and 74% in 2018 and 2019, respectively. This reduction in motility was correlated with damage to mitochondria in M. capitata but not Montipora spp . A major difference between these species is the physiological foundation of their UVR protection, and we hypothesize that UVR protective mechanisms inherent in Montipora spp . mitigate this reproductive damage.
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Different human expectations and environmental ethics are key factors preventing the creation of marine reserve networks. People are skeptical about the benefits of no-take marine reserves because they have adjusted to scarcity and have low expectations about the productive capability of marine ecosystems. Pauly (1995) described this as a shifting baseline in which each generation sets its expectations based on its direct experiences and discounts experiences of previous generations. I show evidence of a declining Caribbean baseline based on Nassau grouper landings from Cuba and the U.S., and review common and often conflicting types of conservation ethics existing in North America. No-take marine reserves can help reestablish human expectations about resource productivity by restoring past conditions in places. Leopold’s biotic ethic provides a framework for achieving sustainable resource use based on laws of ecology and human self-interest. Because changing expectations usually requires direct local experience, education, and changes in conservation ethics, implementing successful marine reserve networks will probably be a slow, incremental process. Establishing no-take reserves can help restore human expectations and provide a common basis for conservation by providing a window to the past and a vision for the future.
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BERLIN-- Edelgard Bulmahn has been a major force in German science and higher education since becoming research minister in 1998. She has proposed an overhaul of Germany's university rules--seeking merit pay and "junior professorships" that would free young scientists to pursue independent research--that has polarized the academic community. In a 9 April interview with Science in her Berlin office, Bulmahn discussed these and other topics in laying out her vision for German research.
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Coral reefs, with their millions of species, have changed profoundly because of the effects of people, and will continue to do so for the foreseeable future. Reefs are subject to many of the same processes that affect other human-dominated ecosystems, but some special features merit emphasis: (i) Many dominant reef builders spawn eggs and sperm into the water column, where fertilization occurs. They are thus particularly vulnerable to Allee effects, including potential extinction associated with chronic reproductive failure. (ii) The corals likely to be most resistant to the effects of habitat degradation are small, short-lived "weedy" corals that have limited dispersal capabilities at the larval stage. Habitat degradation, together with habitat fragmentation, will therefore lead to the establishment of genetically isolated clusters of inbreeding corals. (iii) Increases in average sea temperatures by as little as 1 degrees C, a likely result of global climate change, can cause coral "bleaching" (the breakdown of coral-algal symbiosis), changes in symbiont communities, and coral death. (iv) The activities of people near reefs increase both fishing pressure and nutrient inputs. In general, these processes favor more rapidly growing competitors, often fleshy seaweeds, and may also result in explosions of predator populations. (v) Combinations of stress appear to be associated with threshold responses and ecological surprises, including devastating pathogen outbreaks. (vi) The fossil record suggests that corals as a group are more likely to suffer extinctions than some of the groups that associate with them, whose habitat requirements may be less stringent.