Salm, R.V., S.E. Smith and G Llewellyn. 2001. Mitigating the impact of coral bleaching through marine protected area design. Pp. 81-88 in Schuttenberg, H.Z. (ed.). Coral Bleaching: Causes, Consequences and Response. Selected papers presented at the 9th International Coral Reef Symposium on “Coral Bleaching: Assessing and Linking Ecological and Socioeconomic Impacts, Future Trends and Mitigation Planning.” Coastal Management Report #2230, Coastal Resources Center, University of Rhode Island: 102 pp.

Rodney V. Salm1, Scott E. Smith2, and Ghislaine Llewellyn3



The 1997-1998 El Niño event caused mass coral bleaching of unprecedented proportions. Events of this nature are expected to occur with greater frequency and intensity over the coming decades, which calls for urgent and effective measures to mitigate their impact on coral communities at scales that are significant. Patterns of bleaching and subsequent mortality induced by elevated seawater temperature provide insights into the factors influencing differential susceptibility of coral assemblages to bleaching and mortality.
This paper presents some preliminary ideas on how these patterns might be used to develop selection and design principles for MPAs that enhance survival and recovery prospects for coral communities affected by ENSO-related bleaching. If these principles prove effective, a global review of all coral reef MPAs may required.


Climate Change is likely to have significant impacts on marine biodiversity (Buddemeier, 1993; Hoegh-Guldberg, 1999; Wilkinson, 1996, 1999). Sea level rise will affect turtle nesting beaches, low-lying seabird colonies, and mangroves, to name some of the more obvious probable casualties. Elevated seawater temperature (SSTs), whether or not linked directly to climate change, can cause corals to bleach (Glynn, 1996; Brown, 1997; Hoegh-Guldberg and Jones, 1999) and die and has far reaching impacts on the diversity of dependent organisms.
Large-scale bleaching events have increased in intensity, frequency, and local and geographic distribution in the last two decades (Wilkinson, 1998, 2000). In 1998, the worst year on record, complete loss of live coral in some parts of the world occurred (Goreau et al., 2000). Bleaching spanned the tropics and over 50 countries, proving the global nature of the event (Wilkinson, 2000). Such large-scale bleaching is attributed to thermal stress, in particular to HotSpots4 (Hoegh-Guldberg, 1999), linked to perturbations in normal oceanic or atmospheric circulation patterns. In 1998 the distribution of HotSpots and subsequent bleaching coincided with the largest El Niño Southern Oscillation (ENSO) on record. The massive scale of the 1998 El Niño and 1999 La Niña related coral bleaching and subsequent mortality points to an urgent need for rapid action to mitigate the impact of temperature-induced coral mortality and enhance the prospects for coral recovery (Westmacott et al. 2000).
We now realise that bleaching events and climate change related phenomena pose a serious global threat to coral reefs and need to be incorporated in practical management and planning guideline (Goreau et al., 2000; Westmacott et al., 2000). Our specific interest is how we can help preserve biodiversity in the seas by mitigating the impact of coral bleaching and related mortality through design of marine protected areas (MPAs) (Salm et al., 2000). Although we recognize that active intervention through direct restoration of damaged reef sites is possible and useful in certain circumstances, it is expensive, labor intensive, and limited in scope. We believe that enhancing the prospects for natural recuperation and replenishment through a more passive approach merits serious consideration and could help to achieve recovery of reefs at both sites and scales that are significant given the widespread mortality linked to the 1997-1998 El Niño event.
This paper, presents the concept for a strategy to develop principles that would guide MPA design to enhance survival and natural recovery of coral communities. One goal of the paper is to solicit feedback on the project premise and design, particularly on the merits of these ideas, personal observations on patterns of bleaching-induced coral mortality, and guidance on how to improve upon this initial proposal.


In addition to temperature stress, other potential causative agents of coral bleaching include freshwater flooding, hypersalinity, sedimentation, pollution, oxygen depletion and other physical and chemical stresses (Wesmacott, et al., 2000). Where bleaching is locally restricted, the source of the stress is commonly related to poor management practices in adjacent riparian zones. In such cases, we can intervene directly at the source of the stress (e.g., reforestation and other erosion control measures, etc.) to abate the threat. Such interventions should form part of the reef management practices at any protected area site and are indeed addressed in many integrated coastal management and MPA management programs (Salm et al., 2000).
With large-scale regional or global bleaching events, thermal stress is linked to perturbations in normal oceanic or atmospheric circulation patterns, such as the El Niño Southern Oscillation (ENSO), coupled with rising sea surface temperatures in the tropics (Watson et al. 1996). Where the cause lies with factors that are driving global climate change and global warming, we are powerless to intervene at source to control the stress, at least in meaningful timeframes given the increasing frequency and intensity of these events over the past two decades. The best we can do is to try to mitigate the impact of bleaching induced mortality in two broad ways:
1.      Recognize and protect specific patches of reef where conditions are more likely to ensure low or negligible ENSO related coral bleaching and mortality.
2.      Enhance coral recovery by ensuring conditions are optimal for larval dispersal and recruitment to damaged sites – this will require managing other stresses at these sites (including those that cause bleaching mentioned above and fishing, anchor and diver damage, and waste disposal, among others) and understanding larval dispersal.
The challenge is how to achieve this. The patterns in coral bleaching and related mortality evident since the 1997-1998 El Niño provide some insights.

Susceptibility and Resilience to Bleaching

Despite the widespread mortality that has followed many bleaching events, particularly that of 1998, it is rare for total elimination of living corals to occur. Even in the most severe cases, small patches of reef or individual colonies appear to be more resilient and to survive. In most cases, new coral recruits and recolonization of dead skeletons can be observed within a year after the event. This provides the starting point for regeneration of the reefs. A recent analysis of bleaching reports (Wilkinson, 2000) indicates that there is a wide variability in intensity, species affected, depth, and geographic distribution, and how much mortality a bleaching event causes.
We have observed that individual coral colonies are not equally affected by bleaching, and that colony recovery can be greatly enhanced by the survival of coral tissue in parts of the colony that are more shaded or where particular determinants of what have been called microclimates favor survival. We have observed too that some coral colonies show greater resistance to bleaching and subsequent mortality than others of the same coral species on the same patch of reef.
We also have observed that patches of corals in different parts on the same reef may show greater or lesser susceptibility to ENSO related bleaching and subsequent mortality. This differential response by diverse members of the same coral community to temperature stress provides us with a great opportunity to manage reefs around these pockets of resilience (or lower susceptibility to bleaching and mortality) to enhance the survival and recovery of coral communities and preserve their biodiversity.
In summary, there appear to be both intrinsic physiological factors and extrinsic situational factors that determine a coral’s resilience to bleaching. Intrinsic physiological factors (Rowan et al., 1997) are difficult to control from a spatial management perspective, however differences in bleaching susceptibility due to external environmental factors can be studied and incorporated in management planning. Based on our own observations and conforming with those discussed on the Coral-List (NOAA, 2000), environmental factors that reduce or prevent coral bleaching and related mortality include the following situations:
1.      Areas of upwelling (e.g., corals bleached immediately and comprehensively at one site in the Sultanate of Oman where SSTs reached 39 degrees Celsius in an area of local upwelling and good mixing. Within days the temperature had fallen to back down to 29 degrees Celsius and the corals recovered completely over time) (Salm, 1993; Salm et al., 1993).
2.      Areas with strong currents (e.g., corals in the southern communities where currents are strong in Komodo National Park in Indonesia did not bleach, while those in the sheltered northern reefs exhibited some bleaching (Pet, 1999, pers. com.).
3.      Reefs with emergent corals, which tend to be already stress tolerant (e.g., corals on reef flats in the Rock Islands of Palau (pers. obs.) and Chumbe Island in Tanzania (Riedmiller, 1999, pers. com.) suffered significantly less bleaching than corals down the reef slopes).
4.      Corals which are strongly shaded and protected from prolonged exposure to direct sunlight and UV radiation (e.g., the same species of tabular Acropora and Porites that were severely bleached and evidently dead or dying in the Rock Islands in Palau were alive and healthy in appearance in deeply shaded parts of the same reef) (pers. obs.).
5.      Corals from turbid areas survive better than those in clearer adjacent waters. This is presumably because they are better able to cope with salinity, temperature, and turbidity changes, and may be screened from damaging “sun burn” by refraction and absorption of UV radiation (e.g., Ngeremeduu Bay in Palau where corals were little affected compared to the barrier reef off the bay where coral bleaching and mortality was extensive) (pers. obs.).
Good water mixing and, in certain cases, tolerance of high stress levels seem important in fostering resilience to bleaching and consequent mortality. The impact of elevated SSTs on coral bleaching can be mitigated and recovery enhanced by combinations of the above conditions. For example, reefs around Bali Island showed differences in the onset of bleaching and the rate of recovery that appear linked to currents and upwelling: the colder waters around Nusa Penida appeared to moderate the impact of bleaching and enhance recovery (Sarjena Putra, 2000, pers. com.).
While this is not always the rule, corals in protected areas may fare better than those in unprotected sites. For example, in the 24 months following the 1998 bleaching event along the northern Tanzania coast, corals in reefs closed to fishing by local villagers had almost three times the density of coral recruits compared to open reefs. The reason for this may be that protected areas offer a better supply of larvae for replenishment, and that protected areas relieve anthropogenic pressures on the reef, which might otherwise compound the effect of elevated water temperatures.
There is no immediate cure for coral bleaching. However, these observations indicate that susceptibility to bleaching-induced coral mortality and subsequent recovery differs among similar coral assemblages on the same reef and within the same reef complex. We propose that understanding these patterns of bleaching will provide insights into the environmental determinants of greater or lesser susceptibility to bleaching and will yield some valuable principles for coral reef biodiversity conservation.
Of particular interest to us is how this understanding can yield criteria for reef site selection and guidelines for MPA design that will help to protect resilient coral patches covering the range of reef diversity so that they are able to replenish damaged areas through larval dispersal and recruitment.

Marine Protected Area Selection and Design – A Way Forward?

Field observations support the potential for MPAs to play an increasingly important role in sheltering biodiversity in coral reef ecosystems from climate-related impacts and in the recovery of corals from massive bleaching events. MPAs contribute to reef conservation and management by protecting resilience and areas of undamaged reef and sources of larvae, and by providing areas free of anthropogenic impact with suitable substrate for coral settlement and growth (Salm et al., 2000). However, most current MPAs were not selected or designed with this in mind, nor are they managed specifically for this purpose.
New science-based principles are needed to guide the design and management of MPAs to enable them to maximize coral survival and recovery from bleaching, and to mitigate the adverse impacts of climate-related threats to biodiversity in coral reef ecosystems. For example, zoning schemes or MPA boundaries may need to be revised in order to assure protection for corals more resistant to bleaching, sources for coral recruitment, or areas suitable for coral settlement and growth.
Several efforts to mitigate bleaching related coral mortality are under consideration or are being carried out. In most cases, when mitigation measures are specifically proposed, they include a collage of measures that apply broadly to restoration of reef damage caused by boat anchors, destructive fishing practices, and similar activities, as well as by storm damage (Westmacott et al., 2000). There is nothing proposed that is specific to coral bleaching or that links the patterns of resilience and susceptibility of corals to bleaching induced by SST change with mitigation measures at scales large enough to matter in the face of the challenge.
To address this need, the Asia Pacific Program of The Nature Conservancy and the World Wildlife Fund are planning to jointly develop sound, science-based, empirically-tested principles to guide the selection, design, and management of MPAs to enable them to maximize coral survival and recovery from ENSO related bleaching events. Implementation of these principles represent one, as yet unexplored, means to mitigate the impact of coral bleaching and related mortality and would be expected to increase the prospects for reef survival and recovery. Principles will be developed through the identification of patterns of variation in coral bleaching, resilience, and recovery with respect to external environmental factors. These results will be validated and promulgated as principles for design of marine protected areas that build on resilience and larval dispersal patterns. This endeavor would include five principal activities:
1. Factors that influence bleaching and recovery. The research will begin with a comprehensive survey of 1998 bleaching patterns. The survey will be based on existing reports and analyses, including those prepared by the Global Coral Reef Monitoring Network (GCRMN), papers prepared for the Ninth International Coral Reef Symposium in Bali, and material posted on Coral List. The purpose of this survey is to elaborate the determinants of differential susceptibility of corals to ENSO related bleaching, mortality, and recovery, as outlined above.
2. Study site selection and monitoring methodology. Factors identified through the initial survey will be developed into a set of criteria or hypothesis that can be tested at project study sites. The site selection criteria should capture the range of variables likely to explain differential susceptibility to ENSO related bleaching on coral reefs and the conditions favorable to coral recruitment and recovery. In addition to bleaching susceptibility and recovery criteria, other project design considerations will be addressed as part of study site selection to ensure comparability among sites, including geographic range, existing monitoring arrangements, management effectiveness (e.g., enforcement capabilities, control of impacts from destructive and upstream activities), and variability of context (e.g., reef type, depth, condition, etc.).
In considering the geographic range for the selection of sites, the advantages and disadvantages of a regional or a global focus will be taken into account. A global focus allows a wider range of specific conditions to be included, a larger number of linkages with other organizations and projects to be made (e.g., with the Coral Reef Degradation in the Indian Ocean (CORDIO) project), and an increased chance of observing bleaching events in the near term. On the other hand, a global focus spreads effort and funds widely, which permits less site variety within a relatively small sample, less chance of a single bleaching event affecting all of the sites included in the project, and increases the complexity and costs of project management. To balance these concerns, it is our intention to focus on sites in Indonesia, the Philippines, Fiji, and the Western Pacific.
All study sites will have an existing or imminent monitoring program to reduce project expenses by building on existing activities rather than initiating costly new programs. Also for pragmatic reasons, sites are expected to have a strong TNC, WWF, or partner presence; however, the intention of this decision is not to be exclusive, and we will certainly consider collaboration with other interested parties.
A preliminary list of study site selection criteria include:
·         wide variety of reef types: oceanic, continental, barrier, fringing, patch/pinnacle, atoll
·         varied and strong influence of wind/wave/current regimes
·         wide depth range
·         large tidal range
·         varied orientation: slope, sun/shade
·         presence of natural physico-chemical stresses (e.g., salinity, exposure to air, turbidity)
·         existing monitoring program
·         effective management program.
The research design will be finalized by a few key experts that will: 1) confirm patterns that should be investigated; 2) review study site selection criteria and characteristics and identify 8-10 suitable study reefs; and 3) identify appropriate parameters to monitor and define standard monitoring methods.
3. Preliminary MPA selection, design, and management principles. Field staff at the selected study sites will determine the extent to which current analytical and monitoring efforts include the information needed by the project, and what (if any) changes would be required to carry out the requisite analysis and monitoring. If needed, in depth analysis will be conducted at each study site to describe patterns of bleaching and mortality from the 1998 or last major bleaching event and to identify their likely determinants. From this analysis, and the initial literature and field survey conducted, tentative MPA selection, design, and management principles reflecting the characteristics most conducive to coral survival and recovery from bleaching, will be drafted. These principles will be circulated to a number of scientists and management practitioners, and revised according to the comments received.
4. Monitoring. Field staff at each study site would monitor the rates and nature of recovery from the 1998 bleaching, related to the parameters identified in the selection criteria. While the frequency and method of monitoring will be determined in the final research design, for planning purposes we expect to monitor each site once per year over five years. To the extent possible, this monitoring will be included in regular activities already being carried out at existing project sites. Annual reports of monitoring results across the study sites, and at specific sites of comparable size in the Great Barrier and Meso-American Barrier Reefs, for the sake of comparison, would be produced and widely disseminated for comment.
5. Revalidation and promulgation. A detailed analysis of the patterns of coral bleaching, survival, and mortality during the next major ENSO-related bleaching event will be conducted at each study site. On the basis of these analyses, a determination will be made as to the extent the preliminary management principles were validated by this new bleaching event. If they prove to be generally robust, the principles would then be revised, as needed, and disseminated widely for use as guidelines for marine protected area managers throughout the Asia Pacific region and worldwide.


Measures to mitigate the impact of ENSO-related mass coral bleaching need to be significant at the scale witnessed following the 1997-1998 El Niño. A combination of rigorous protection of areas where corals show greater resilience to bleaching with measures to enhance natural recovery of adjacent areas where corals are more susceptible to bleaching and related mortality could provide a solution. As a start, new science-based, empirically-tested principles are needed to guide the selection, design and management of MPAs so that they can maximize coral survival and recovery from ENSO-related bleaching events.


Brown, B.E. 1997. Coral Bleaching: Causes and consequences. Coral Reefs, 16 Suppl.: S129-S138.
Buddemeier, R.W. 1993. Corals, climate and conservation. Proc. 7th Inter. Coral Reef Symp., 1: 3-10.
Glynn, P.W. 1990. Global Ecological Consequences of the 1982-83 El Nino – Southern Oscillation. Elsevier, Amsterdam: 563 pp.
Glynn, P.W. 1996. Coral Reef Bleaching: facts, hypotheses and implications. Global Change Biology, 2: 495-509.
Goreau, T.J., McClanahan, T., Hayes, R., and Strong, A.E. 2000. Conservation of Coral Reefs after the 1998 global bleaching event. Conservation Biology, 14: 5-15.
Goreau, T.J., and Hayes, R., 1994. Coral Bleaching and Ocean HotSpots. Ambio 23: 176-180.
Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world’s coral reefs. Marine and Freshwater Research, 50: 839-866.
Hoegh-Guldberg, O., and Jones, R. 1999. Photo-inhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Marine Ecology Progress Series, 183: 73-86.
National Oceanic and Atmospheric Administration (NOAA). 2000. Coral-List archive.
Rowan, R., Knowlton, N., Baker, A., and Jara, J. 1997. Landscape ecology of algal symbionts creates variation within episodes of coral bleaching. Nature, 388: 265-269.
Salm, R.V. 1993. Coral reefs of the Sultanate of Oman. Atoll Res. Bull., 380: 85 pp.
Salm, R.V., Jensen, R.A.C., and Papastavrou, V.A. 1993. Marine Fauna of Oman: Cetaceans, Turtles, Seabirds, and Shallow Water Corals. A Marine Conservation and Development Report. IUCN, Gland, Switzerland: vi + 66 pp.
Salm R.V., Clarke J.R., and E. Siirila. 2000. Marine and Coastal Protected Areas: A Guide for Planners and Managers. IUCN. Washington DC, USA: 371 pp.
Watson, R.T., Zonyowera, M.C., and Moss, R.H. 1996. Climate Change 1995: Impacts, Adaptations and Mitigation of Climate Change: Scientific-Technical Analyses. Contribution of Working Group II to the Second Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York, New York: 889 pp.
Westmacott, S., Teleki, K., Wells, S., and West, J. 2000. Management of bleached and severely damaged coral reefs. IUCN, Gland, Switzerland: 36 pp.
Wilkinson, C.R. 1996. Global change and coral reefs: impacts on reefs economics and human cultures. Global Change Bioogy., 2: 547-558.
Wilkinson, C. (ed.). 1998. Status of Coral Reefs of the World: 1998. Australian Institute of Marine Science, Queensland, Australia: 184 pp.
Wilkinson, C.R. 1999. Global and local threats to coral reef functioning and existence: review and predictions. Marine and Freshwater Research, 50: 867-878.
Wilkinson, C. (ed.). 2000. Status of Coral Reefs of the World: 2000. Australian Institute of Marine Science, Queensland, Australia: 363 pp.

1 The Nature Conservancy, 923 Nu’uanu Ave, Honolulu 96817, U.S.A. (
2 The Nature Conservancy, 4245 N Fairfax Drive, Arlington VA 22203-1606, U.S.A. (
3 World Wildlife Fund, 1250 Twenty-Fourth St., NW, Washington DC 20037-1132, U.S.A.
4 A HotSpot is an area where sea surface temperatures (SSTs) have exceeded the expected yearly maximum (the highest temperature per year, averaged for a 10 year period) for that location (Goreau and Hayes, 1994).