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Global Trajectories of the Long-Term Decline of Coral Reef Ecosystems

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Science  15 Aug 2003:
Vol. 301, Issue 5635, pp. 955-958
DOI: 10.1126/science.1085706

Abstract

Degradation of coral reef ecosystems began centuries ago, but there is no global summary of the magnitude of change. We compiled records, extending back thousands of years, of the status and trends of seven major guilds of carnivores, herbivores, and architectural species from 14 regions. Large animals declined before small animals and architectural species, and Atlantic reefs declined before reefs in the Red Sea and Australia, but the trajectories of decline were markedly similar worldwide. All reefs were substantially degraded long before outbreaks of coral disease and bleaching. Regardless of these new threats, reefs will not survive without immediate protection from human exploitation over large spatial scales.

Coral reefs and associated tropical nearshore ecosystems have suffered massive, long-term decline in abundance, diversity, and habitat structure due to overfishing and pollution (17). These losses were more recently compounded by substantial mortality due to disease and coral bleaching (812). Although much longer records exist for some coral (13) and commercially important fisheries species (2, 3), detailed ecological descriptions of reef ecosystems are less than 50 years old (14, 15). The long-term historic sequence of ecosystem decline is unknown for any reef, thereby obscuring the potential linkage and interdependence of the different responsible factors that must be unraveled for successful restoration and management.

We reconstructed the ecological histories of 14 coral reef ecosystems worldwide (16) using consistent criteria throughout. We determined the ecological status of reefs ranging from pristine to globally extinct (Table 1) for seven general categories of biota (hereafter referred to as guilds) (17) for each of seven culturally defined periods ranging from prehuman to the present (table S1) (18). We used cultural periods rather than calendar years because the magnitude of human impacts depends primarily on technological prowess and economic structures that were out of phase geographically until converging in the 20th century. Guilds and ecological status were broadly defined so that the same standards could be used for all periods and regions examined and so that widely disparate paleontological, archaeological, historical, fisheries, and ecological data could be used in the same analysis (tables S2 and S3) (17).

Table 1.

Ecological states and criteria used to assess the 14 tropical marine sites analyzed.

Ecological state Criteria for classification
Pristine Detailed historical record of marine resource lacks any evidence of human use or damage.
Example: Fossil coral assemblages
Abundant/common Human use with no evidence of reduction of marine resource.
Example: No reduction in size of fish vertebrae in middens or relative abundance of species
Depleted/uncommon Human use and evidence of reduced abundance (number, size, biomass, etc.).
Examples: Shift to smaller sized fish; decrease in abundance, size, or proportional representation of species
Rare Evidence of severe human impact.
Examples: Truncated geographic ranges; greatly reduced population size; harvesting of pre-reproductive individuals
Ecologically extinct Rarely observed and further reduction would have no further environmental effect.
Examples: Observation of individual sighting considered worthy of publication; local extinctions
Globally extinct No longer in existence.
Example: Caribbean monk seal

The average ecological status of each guild for all regions combined (17) declined sharply over time (Fig. 1). In general, large animals declined faster than small animals and free-living animals declined more rapidly than architectural builders such as seagrasses and corals. Large carnivores and herbivores were almost nowhere pristine by the beginning of the 20th century, when these guilds were already depleted or rare in more than 80% of the 14 regions examined. The universal lag in decline of architectural guilds is consistent with earlier observations for Caribbean reefs (19).

Fig. 1.

(A to G) Ecological change in coral reef guilds through time. Time trajectories of ecological condition for each of seven guilds of reef inhabitants (17) expressed as the percentage of regions in each ecological state from 14 regions (16) in the tropical western Atlantic, Red Sea, and northern Australia. Cultural periods (18): P, prehuman; H, hunter-gatherer; A, agricultural; CO, colonial occupation; CD, colonial development; M1, early modern; M2, late modern to present.

We used principal components analysis (PCA) to ordinate the data and to describe the historical trajectories of change within each region in terms of the ecological status of all seven guilds combined (17). Reef regions were defined as pristine for the initial (prehuman) period, and for purposes of comparison, we included a hypothetical reef for which all seven guilds were ecologically extinct. Only the first principal component (PC1) was interpretable (17). The resulting trajectories (Fig. 2A) closely and consistently track PC1, which explains 91% of the total variation in the data. The key structures in the data set were thus effectively captured by a one-dimensional system, with each region's time periods mostly sequentially ordered along PC1, which is described overwhelmingly by the status of large herbivores and carnivores (20).

Fig. 2.

PCA of ecosystem degradation based on the ecological state of all seven guilds of reef inhabitants at the 14 reef regions. Only PC1 was significant (17). (A) Time trajectories for each reef region over seven cultural periods. Each reef started at a single point to the left in the PCA space that is the pristine ecosystem state (Table 1) (17). Trajectories are mostly monotonic through time, but minor reversals occur in four regions (denoted with an “x” in the filled circle). The hypothetical ecologically extinct state, on the right, is one in which all seven guilds are ecologically extinct. PC1 is interpreted as an axis of historical degradation over time measured in cultural periods. The most important guilds influencing the trajectories of decline are large herbivores and carnivores (20). (B) End points (present ecosystem condition) of the 14 reef regions plotted along an axis of ecosystem degradation measured as the relative distance along PC1 between pristine and ecologically extinct. Oceanic regions are color coded: Australia, blue; Red Sea, green; western Atlantic, purple. OGBR, outer Great Barrier Reef; IGBR, inner Great Barrier Reef; TORS, Torres Strait Islands; S.RED, southern Red Sea; N.RED, northern Red Sea; BELI, Belize; BERM, Bermuda; CAYM, Cayman Islands; BAHA, Bahamas; E.PAN, eastern Panama; MORB, Moreton Bay; USVI, U.S. Virgin Islands; W.PAN, western Panama; JAMA, Jamaica.

PCA also provides a simple, objective index of present-day reef degradation as measured by the normalized scores for the end points of each regional trajectory along PC1 (Fig. 2B). As expected, reefs in the western Atlantic have declined more severely than in Australia or the Red Sea. The best-protected reefs in the world, on the Great Barrier Reef, are the closest to pristine. But these same reefs are also one-quarter to one-third of the way along PC1 to ecological extinction. Moreover, the reefs of Moreton Bay, at the extreme southern end of the Great Barrier Reef, are as close to ecological extinction for all seven guilds as the severely degraded reefs of eastern Panama and the Virgin Islands.

The overall historical trajectory of reef degradation across all cultural periods is markedly linear, despite the wide range of values within any one cultural period (Fig. 3). Most importantly from the perspective of reef conservation and management, most of the reef ecosystems were substantially degraded before 1900. Recent widespread and catastrophic episodes of coral bleaching and disease have distracted attention from the chronic and severe historical decline of reef ecosystems (10, 2123). However, all of the reefs in our survey were substantially degraded long before the first observations of mass mortality resulting from bleaching and outbreaks of disease (10, 11). The only reasonable explanation for this earlier decline is overfishing (3), although land-derived pollution could have acted synergistically with overfishing in some localities.

Fig. 3.

Percent degradation of 14 reef regions over time. Data for each cultural period are derived from the PCA analysis plotted in Fig. 2A as measured along PC1 as the axis of reef degradation. Each point represents percent degradation of a particular site at a particular time. Numbers in parentheses are the numbers of reef regions recorded for each cultural period (17). Linear regression is plotted along with the 95% confidence interval. Abbreviations for cultural periods are as in Fig. 1.

Historical trajectories of reef degradation provide a powerful tool to explain global patterns and causes of ecosystem collapse, as well as to predict future ecosystem states, allowing managers to anticipate ecosystem decline through an understanding of the sequence of species and habitat loss. Management options will vary among regions, but there must be a common goal of reversing common trajectories of degradation. The maintenance of the status quo within partially protected areas such as the Great Barrier Reef is at best a weak goal for management, which should strive instead for restoring the reefs that are clearly far from pristine. Regardless of the severity of increasing threats from pollution, disease, and coral bleaching, our results demonstrate that coral reef ecosystems will not survive for more than a few decades unless they are promptly and massively protected from human exploitation.

Supporting Online Material

www.sciencemag.org/cgi/content/full/301/5635/955/DC1

Materials and Methods

Tables S1 to S3

References and Notes

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