• coral;
  • climate change;
  • gardening concept;
  • Philippines;
  • restoration


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments

Restoration of coral reefs is generally studied under the most favorable of environmental conditions, a stipulation that does not always reflect situations in the field. A 2-year study (2005–2007), employing the “reef gardening” restoration concept (that includes nursery and transplantation phases), was conducted in Bolinao, Philippines, in an area suffering from intense human stressors. This site also experienced severe weather conditions, including a forceful southwesterly monsoon season and three stochastic environmental events: (1) a category 4 typhoon hit the Bolinao's lagoon (May 2006) impacted farmed corals; (2) heavy rains (August 2006) caused seepages of freshwater, followed by reduced salinity that impacted transplanted colonies; and (3) a bleaching event (June 2007) caused by warming of seawater, severely impacted both nursery and transplanted corals. This study analyzes the effects of these natural catastrophes on restoration efforts, and presents the successes and failures of recently used restoration instruments. Our results show that (1) in the nursery phase, consideration should be paid to depth-flexible constructions and tenable species/genotypes prioritization and (2) for transplantation acts, site/species deliberation, timing, and specific site selections should be taken into account. Only the establishment of large-scale nurseries and large transplantation measures and the adapting of restoration management to the frequently changing environment may forestall extensive reef degradation due to the combination of continuous anthropogenic and worsening global changes.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments

Global climate predictions foretell more frequent and intense catastrophic environmental events (Easterling et al. 2000) that may eventually lead to the destruction of ecosystems through habitat loss and elimination of key species (Allison et al. 2003). Prevailing management considerations refer to the impacts of extreme climatic events, such as large-scale coral bleaching episodes and associated reef dwelling mortalities, as unpredictable forces, influencing habitats beyond the control of local management plans and undermining the achievement of assigned management aims (Mumby & Steneck 2008). However, a modified outlook could employ methodologies that allow the probability of catastrophic disturbances to be incorporated into site selection without enforcing additional conservation efforts (Game et al. 2008; Baskett et al. 2009). To date, there has been little discussion of the impacts of unpredictable forces on the design and execution of long-term restoration of coral reef ecosystems.

Coral reefs are highly important to the ecosystem health and economy of many tropical and subtropical nations (Gomez 1997; Moberg & Folke 1999; Hughes et al. 2003), and have been badly impacted by a combination of human and natural disturbances. For example, Bruno and Selig (2007) pointed to a decline in the Indo-Pacific coral coverage from 42.5 to 22.1%, in the short period from the early 1980s to 2003. An increasing number of publications state that the risks to coral reefs are associated not only with anthropogenic impacts but also with the mounting frequency and intensity of global changes in climate (Pittock 1999; Jackson et al. 2001; Hughes et al. 2003; Wakeford et al. 2008; Baskett et al. 2009) causing variable damages, such as increasing coral reefs bleaching events (Hoegh-Guldberg 1999). Impacts on other ecosystems may also affect coral reefs indirectly. Elevated global temperature causing the increase in global hydrological cycle due to evaporation, may cause successive events of strong rainfall (Pittock 1999) which, in turn, lead to an influx of freshwater that can harm coral reefs by reducing salinity, and to land erosion which increases turbidity and pollution. Therefore, it is necessary to understand the actual impacts of climate changes on coral reefs and revise the essential management protocols to counter them.

The rapid degradation of reef ecosystems may override the system's capacity to regenerate adequately (Chadwick-Furman 1996; Hodgson 1999; Wilkinson 2002; Rinkevich 2005, 2006, 2008; Manning et al. 2006) causing dramatic, long-lasting, and perhaps irreversible shifts in species composition (Scheffer et al. 2001; Folke et al. 2004). This foreteller dismal fate for reef degradation has initiated the suggestion that the future of coral reefs should be focused on restoration, an active management instrument (Rinkevich 2008). Coral transplantation is a major tool in active reef rehabilitation strategies (Yap 2003; Rinkevich 2006). In this study the rationale emerges from the “gardening concept,” which comprises two working phases (Rinkevich 1995, 2000, 2005, 2006). The first phase is the establishment of in situ nurseries (preferably mid-water floating nurseries [Shafir et al. 2006a, b]) in which large numbers of coral fragments are reared to sizeable coral colonies under controlled and favorable conditions. The second phase is engaged with the transplantation of these nursery-grown coral colonies onto denuded natural habitats (Rinkevich 1995, 2000, 2005, 2006; Epstein et al. 2001). The nursery phase of the “gardening concept” proved to be highly successful in areas less frequented by catastrophic events (Epstein et al. 2001; Soong & Chen 2003; Shafir et al. 2006a; Putchim et al. 2008). However, detailed studies that evaluate the performance of the concept in reefs affected by severe weather conditions, or prolonged environmental stressors, have yet to be carried out.

From July 2005 to July 2007 a restoration study, using both phases of the “gardening concept,” was performed in shallow reef areas in Bolinao, Philippines. During this period, the area experienced extreme weather conditions brought about by southwesterly monsoons and three stochastic natural catastrophes, which harmed nursery-farmed corals and transplants. In May 2006, a category “4” typhoon (Typhoon Caloy) struck Bolinao. In August 2006, an above average lengthy rainy period caused seepage of freshwater from the ground, in several locations along the transplanted area. In June 2007, elevated seawater temperature, unusually low tide and high radiation, caused mass coral bleaching. Here we outline the effects of these natural stressors on the two-phase restoration protocols with an eye to amending reef-restoration measures and the use of proactive threats-based approach in reef restoration. As suggested by Grigg and Dollar (1990), we referred to the stress forces outcomes with a single major parameter, mortality rate, where the degree of mortality reflects the intensity of stress (Grigg & Dollar 1990).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments

Study Sites

The study was conducted at Cape Bolinao, Pangasinan, a coastal town in northwestern Philippines, on the eastern coast of the South China Sea. Bolinao, which lies between 16°22′ and 16°27′N latitude and between 119°52′ and 120°00′E longitude (Fig. 1), experiences the southwesterly monsoon from June to October, the northeasterly monsoon from November to March, and weak easterlies from April to May. The fringing reefs of Bolinao, reaching 30 m depth with average live coral cover of 20%, have been subjected to destructive fishing practices (Gomez 1997, 2001; Raymundo et al. 2007), eutrophication (Diego-McGlone et al. 2008), and to natural disturbances such as strong tropical storms (Puotinen 2007).


Figure 1. Bolinao, Pangasinan, Philippines, and detailed study sites: site 1, “Silaqui” nurseries location; site 2, “Malilnep channel” transplantation site for P. damicornis, M. digitata, and A. formosa; site 3, “Binabalian Labas” transplantation site for E. lamellosa, M. scabricula, and P. rus; site 4, “Coral Garden” transplantation site for M. digitata.

Download figure to PowerPoint

Our study was conducted at four sites along the Santiago lagoon, site 1 served as the nursery-based area and in sites 2–4, 1-year old nursery-grown corals (NGCs) were transplanted onto bare knolls (Fig. 1). At site 1 the coral nurseries faced the north shore of Silaqui Island, in a shallow, sandy bottom area of the lagoon (2–4 m depth). The site 2 formed part of the barrier reef at the inner mouth of the “Malilnep” Channel connecting the lagoon to the sea, a 3-m deep reef flat, dominated by branching and massive coral species (Acoporids, Pocilloporids, and Poritids). This site is subjected to wave activity and strong currents during SW and NE monsoon seasons. The site 3, “Binabalian Labas” on the west side of Santiago Island, was at a maximal depth of 6 m (the deeper site) and 300 m from the Santiago Island, an area with scattered, bare coral knolls, and little live coral cover. This site is located nearer to the Island shore, in a bay created by the Santiago Island, which protects it from the SW and NE monsoons. The site 4, the “Coral Garden” on the northeast of Santiago Island, was located further inside the lagoon, a shallow water area (3–2 m depth) with sandy bottom and patches of coral rubble exposed to the NE monsoon but more protected from the SW monsoon.

Study Procedures

During July and August 2005, two nurseries were constructed, holding 6,824 coral ramets from seven coral species (Merulina scabricula, Montipora digitata, Echinopora lamellosa, Pocillopora damicornis, Porites rus, Acropora formosa, and M. aequituberculata, Table 1; Shaish et al. 2008). For each species, the two to three–donor colonies chosen in the field as a source for ramets were considered as different genotypes (Shaish et al. 2008). The nurseries with farmed corals were maintained and monitored once a month for 1 year by a team of three divers (Shaish et al. 2008). One year later (August 2006), NGC colonies were transplanted onto several bare-of-corals knolls. The knolls were rock structures, comprising dead coral skeletons, mainly those of massive corals. Chosen knolls were selected according to their size, raising about 0.5 m above substrate and with at least 2 m2 of flat top area. Most large fouling organisms growing on top of the knolls (algae, sponges, tunicates) were removed prior to transplantation. Distances between knolls ranged from 5 to 20 m.

Table 1.  Composition and numbers of eight coral species used in the study; additional details for the nursery in Shaish et al. (2008). NGCs—nursery-grown coral colonies.
SpeciesM. scabriculaM. digitataE. lamellosaP. damicornisP. rusA. formosaM. aequituberculataH. coerulea
  1. aM. scabricula, E. lamellosa, P. rus, and M. aequituberculata: aerial surface area (cm2); M. digitata, P. damicornis, and A. formosa: height (cm).

  2. bIn site 2, five knolls were transplanted with M. digitata colonies and in site 4, four knolls.

Ramets deployed in nurseries, first year1,2601,9602,030570354333317
Donor genotypes (Nursery 2005)2332111
NGCs transplanted onto knolls3636036036036360
Average NGCs size at transplantationa12 ± 510 ± 317 ± 55 ± 110 ± 516 ± 5
Distance between corals on the knoll (cm)10206101020
“Mono” species knolls099900
Colonies per knoll363636
“Poly” species knolls333333
Colonies per knoll121212121212
Location of transplanted knollssite 3site 2b site 4site 3site 2site 3site 2
Colonies left in nursery after transplantation4331,3811,066251283251189
New ramets deployed00082254300210
New genotypes (Nursery 2006)00033001

The colonies belonging to two branching forms, M. digitata and P. damicornis, and one encrusting form, E. lamellosa, showed the highest growth and survivorship rates under our nursery conditions and provided the largest number of NGCs ready for transplantation (Shaish et al. 2008). These species were subjected to mono-species transplantation experiments; in each plot, only single species colonies were transplanted. Poly-species transplantations (i.e. in each plot, colonies of more than one species were attached side by side) were divided into two types, one holding fast-growing, branching species (M. digitata, P. damicornis, and A. formosa) and the other, slow-growing, encrusting, submassive and leaf-like species (E. lamellosa, P. rus, and M. scabricula). NGCs (n = 1188) were transplanted onto bare knolls (n = 33) in three locations inside the lagoon (sites 2, 3, and 4; Table 1; Fig. 1), at a density of 36 colonies per knoll. The fast-growing species combinations were transplanted into the shallower sites (sites 2 and 4) and the slow-growing species combinations into the deeper site (site 3). This selection was based on the abundance of these species on the reef. Knolls' location and corals' distribution are depicted in Table 1.

The transplantation was designed as a grid of 6 × 6 colonies. The branching coral species, grown inside plastic tubes in the nurseries (Shaish et al. 2008), were transplanted by inserting the plastic tubes into holes chiseled in the substrate and secured with small amounts of “Aquamend” glue. The encrusting, submassive, and leaf-like species, which grew in the nursery on small pieces of plastic mesh (Shaish et al. 2008), were attached to the substrate, each by two small umbrella nails on two sides. During October 2006, the nurseries were renovated and refilled. Colonies not used for transplantation were left on the nursery for another year. Heliopora coerulea was added to the nursery and new donor colonies of P. damicornis and P. rus were selected for creating new ramets (Table 1).

Environmental Disturbances

During the course of this study, several stochastic natural catastrophic events affected the area of Bolinao lagoon (Fig. 2): (1) on 12–15 May 2006, 9 months after establishing the coral nurseries, Typhoon Caloy hit the Philippines, reaching 150 km/hour in the South China Sea and raising powerful waves inside the Santiago lagoon (Fig 2). (2) During 13–24 August 2006, 2 weeks after transplantation, heavy precipitation occurred over the Pangasinan province (including Bolinao, Fig. 2), with a record rainfall of 274.3 mm (×1.5 times that of rainfall in 2005: Consequently, we observed foci of freshwater underground seepage within the lagoon, mainly in sites 2 and 3, in the vicinity of the transplantation knolls. At the end of August 2006, seawater around nine knolls were sampled: six knolls at site 2, five carrying P. damicornis transplants, and one with poly-species transplants (M. digitata, A. formosa, and P. damicornis); three knolls at site 3, two with E. lamellosa transplants and one with poly-species transplants (E. lamellosa, P.rus, and M. scabricula). The knolls were selected in areas where we documented murky waters. Salinity was measured with a portable refractometer (Reichert-Jung; accuracy ±0.05 ppt). (3) From September until November 2006, during the southwest monsoon of 2006, tempestuous weather consisting of three regular typhoons, two tropical depression storms, and two super Typhoons hit the Philippines (Super typhoon Paeng on October 27–31, and Super typhoon Reming on November 28 to December 8,, Fig. 2). (4) On 16 June 2007, 10 months after transplantation, an extremely low tide combined with clear skies and high irradiation, rapidly raised surface water temperature to approximately 33°C. This combination of high temperature and radiation led to mass coral bleaching in the lagoon and in the fringing reef surrounding it. Bleaching was observed down to 7-m depth.


Figure 2. Chronological illustration for restoration operation dates (regular) and major weather events (bold). 1, monitoring dates for nursery; 2, monitoring dates for transplanted colonies.

Download figure to PowerPoint

All weather data on typhoons and rainfall were supplied by the Philippine weather site Local scientists at the Bolinao Marine Station supplied data on water temperatures.

Maintenance and Monitoring

In the first year, the nurseries were monitored monthly (Fig. 2). Dead, missing, and bleached ramets were counted. The dead ramets were removed from the trays to avoid recounting in successive monitoring sessions. Growth rates of 10 tagged fragments from each donor genotype were photographed monthly with a digital Olympus camera using a side ruler for calibration. Monthly maintenance of the nurseries also included fixing of damaged/worn-out parts and removal of settled macroalgae around growing corals. In the second year, the transplanted colonies and nurseries were monitored every 3 months for 1 year (August 2006–July 2007). A team of two divers recorded the number of dead, detached, partially dead and bleached (of the survived colonies) colonies. Dead colonies in the transplantation experiment were not removed from the plots.


Mean percent mortality, detachment, partial mortality, and bleaching were calculated after each monitoring date and referred to the preceding month. Statistical tests were performed using SPSS software. In these tests, one preliminary assumption was tested: the existence of homogeneity of variance (Underwood 1981). Homogeneity of variance was checked using Levene's test. When the data failed to correspond with the assumption, non-parametric tests (e.g. Mann–Whitney U test, Kruskal–Wallis test, and Wilcoxon signed ranks test) were performed.

The effects of disturbances were analyzed in two ways, one by including the results of all the species together exhibiting and overall effects on nursery and transplantation, and the second by calculating the results for each specific species, pointing out species resistance and recovery abilities.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments

Typhoon Impacts on Farmed Corals

In July 2005, two in situ corals nurseries holding 6,824 coral ramets from seven species were constructed in a shallow lagoon at 2-m depth and monitored over 1 year (results for mortality, detachment, and growth per species are summarized in Table 2). Eight months after the nurseries were established a super typhoon (Typhoon Caloy, 9–15 May 2006, Fig. 2) hit the area. Overall average monthly mortality during the pre-typhoon period (August 2005–April 2006) was 0.55 ± 0.47% (n = 324 colonies), significantly lower from the post-typhoon (May and June 2006; n = 219 colonies) values of 2.11 ± 2.05% (Wilcoxon signed ranks test; p < 0.05, Tables 2 & 3). Concerning species-specific mortality, an increased post-typhoon mortality was recorded in all species (Table 2), with statistically significant values for Merulina scabricula and Echinopora lamellosa (Wilcoxon signed ranks test; p < 0.05, Table 3).

Table 2.  Mortality, detachment and growth for 1 year nursery farmed coral colonies; averages represent coral genotypes within a species; values for P. rus, A. formosa, and M. aequituberculata are for a single genotype in one nursery; average values therefore were not calculated for these species; growth of branching species was calculated as percentages of height added and for massive/encrusting species as percentage of area added (Shaish et al. 2008); in May 2006, monitoring was performed 10 days after the typhoon (in bold).
DateSpecies-Specific Values
M. digitataE. lamellosaP. damicornisM. scabriculaP. rusA. formosaM. aequituberculata
  1. n.d = no data were calculated.

Mortality (%)
August 050.1 ± 0.20.4 ± 0.65.7 ± 4.60.2 ± 0.218.900
September 0500.1 ± 0.200.4 ± 0.55.600
October 050.1 ± 0.30.6 ± 1.30.6 ± 0.82.2 ± 2.13.300.3
November 050.0 ± 0.10.5 ± 0.50.4 ± 0.91.9 ± 1.52.800
December 0500.5 ± 0.90.2 ± 0.40.3 ± 0.20.800
January 060.1 ± 0.20.1 ± 0.200.4 ± 0.3000
February 0600.9 ± 1.00.4 ± 0.90.4 ± 0.81.700
March 060.1 ± 0.20.1 ± 0.20.2 ± 0.50.6 ± 0.5001.0
April 0600.6 ± 0.50.1 ± 0.30.5 ±
May 061.6 ± 2.11.0 ± 1.52.0 ± 2.614.2 ±
June 0600.5 ± 0.60.1 ± 0.31.6 ± 2.7004.6
Detachment (%)
August 050.4 ± 0.31.2 ± 0.60.2 ± 0.40.6 ±
September 050.2 ± 0.30.2 ± 0.300.8 ± 0.8000
October 050.1 ± 0.21.8 ± 2.01.1 ± 1.63.3 ± 3.32.600.3
November 050.3 ± 0.61.0 ± 1.30.4 ± 0.94.6 ± 5.12.000
December 050.1 ± 0.40.3 ± 0.70.6 ± 1.30.3 ± 0.5000.3
January 0600.4 ± 0.40.2 ± 0.51.3 ± 2.10.400.6
February 0600.4 ± 0.400.7 ± 0.80.800
March 0600.3 ± 0.600.4 ± 0.5000
April 0600.1 ± 0.201.2 ± 1.5000
May 0611.6 ± 28.4000000
June 060.2 ± 0.50.4 ± 0.600.7 ± 1.0000.3
Growth Added (%)
September 0548 ± 3752 ± 26n.d17 ± 1753 ± 30n.d61 ± 25
October 0514 ± 1828 ± 24n.d16 ± 1710 ± 15n.d21 ± 21
November 0516 ± 1317 ± 1360 ± 328 ± 192 ± 21n.d−0.3 ± 15
December 058 ± 1210 ± 1317 ± 15−1 ± 1233 ± 12n.d6 ± 11
January 06n.dn.dn.dn.dn.dn.dn.d
February 0626 ± 2619 ± 2232 ± 270.2 ± 217 ± 21n.d3 ± 16
March 0627 ± 3015 ± 1019 ± 1712 ± 17n.d10 ± 120.4 ± 14
April 0610 ± 1513 ± 137 ± 11−2 ± 14n.d12 ± 8−7 ± 30
May 06−2 ± 23−2 ± 1011 ± 12−4 ± 18−9 ± 156 ± 7−29 ± 14
June 063 ± 144 ± 11−4 ± 102 ± 123 ± 12−3 ± 5−15 ± 30
Table 3.  Summary of statistical analyses for the impacts of environmental catastrophes on nurseries and transplanted corals at Bolinao, Philippines (years 2006, 2007). Bold numbers point to significant differences.
Typhoon Caloy (May 2006) Impact on NurseriesMortality (%)Detachment (%)Bleaching (%)Growth (%)
OverallBefore0.6 ± 1.80.5 ± 1.31.6 ± 3.619 ± 24
 After2.1 ± 5.71.7 ± 10.31.5 ± 3.90.3 ± 15
M. digitataBefore0.1 ± 0.20.1 ± 0.33.5 ± 4.920 ± 25
 After0.8 ± 1.65.9 ± 20.10.2 ± 0.70.1 ± 20
E. lamellosaBefore0.4 ± 0.70.6 ± 1.00.3 ± 0.521 ± 22
 After0.8 ± 1.10.2 ± 0.41.6 ± 2.01 ± 11
P. damicornisBefore0.9 ± 2.30.3 ± 0.80.5 ± 0.926 ± 28
 After1.1 ± 2.0004 ± 13
M. scabriculaBefore0.8 ± 1.11.5 ± 2.51.4 ± 3.17 ± 18
 After7.9 ± 12.30.3 ± 0.70.2 ± 0.4−1 ± 15
P.rusBefore3.8 ± 6.00.7 ± 1.04.7 ± 7.421 ± 27
 After1.1 ± 1.503.3 ± 0.3−3 ± 14
A. formosaBefore0.0 ± 0.10.1 ± 0.21.0 ± 2.611 ± 10
 After0.8 ± 1.1010.0 ± 13.72 ± 8
M. aequituberculataBefore0.1 ± 0.30.3 ± 0.40.7 ± 2.212 ± 29
 After2.5 ± 3.00.2 ± 0.28.5 ± 12.0−22 ± 23
SW monsoon (November 2006) Impact on TransplantsMortality (%)Detachment (%)  
OverallNovember 200647 ± 3910 ± 15  
 February/May 200738 ± 439 ± 23  
site 2November 200656 ± 3712 ± 18  
 February/May 200739 ± 4214 ± 30  
site 3November 200646 ± 415 ± 7  
 February/May 200752 ± 453 ± 10  
site 4November 20061 ± 118 ± 7  
 February/May 20071 ± 30  
M. digitataNovember 200641 ± 4011 ± 13  
 February/May 200719 ± 3513 ± 27  
P. damicornisNovember 200668 ± 3214 ± 22  
 February/May 200758 ± 427 ± 27  
A. formosaNovember 200648 ± 4711 ± 19  
 February/May 200744 ± 3953 ± 41  
E. lamellosaNovember 200659 ± 364 ± 7  
 February/May 200786 ± 270  
M. sacbriculaNovember 200642 ± 513 ± 5  
 February/May 20076 ± 716 ± 19  
P. rusNovember 200609 ± 9  
 February/May 200725 ± 400  
Bleaching Event (June 2007) Impact on TransplantsMortality (%)Detachment (%)Partial Mortality (%)Bleaching (%)
OverallFebruary/May 200739 ± 439 ± 2400
 July 200713 ± 287 ± 2223 ± 31100 ± 0
site 2February/200741 ± 4215 ± 3100
 July 200727 ± 362 ± 542 ± 35100 ± 0
site 3February/May 200752 ± 453 ± 1000
 July 2007000100 ± 0
site 4February/May 20071 ± 3000
 July 2007026 ± 4321 ± 25100 ± 0
Bleaching Event (June 2007) Impact on NurseriesMortality (%)Detachment (%)Partial Mortality (%)Bleaching (%)
OverallDecember 2006/March 20076 ± 101 ± 22 ± 40.4 ± 1
 June/July 20079 ± 160.6 ± 215 ± 2579 ± 34
A. formosaDecember 2006/March 20075 ± 40.3 ± 0.72 ± 40.5 ± 0.6
 June/July 200741 ± 4600.5 ± 180 ± 19
E. lamellosaDecember 2006/March 20073 ± 42 ± 23 ± 61 ± 3
 June/July 20079 ± 61 ± 222 ± 2479 ± 13
H. coeruleaDecember 2006/March 20071 ± 30.7 ± 0.81 ± 30
 June/July 20074 ± 62 ± 407 ± 13
M. aequituberculataDecember 2006/March 200714 ± 1506 ± 80.5 ± 1
 June/July 200721 ± 2005 ± 1193 ± 9
M. digitataDecember 2006/March 20070.3 ± 0.50.1 ± 0.20.7 ± 20.1 ± 0.4
 June/July 20070.4 ± 0.60050 ± 53
M. scabriculaDecember 2006/March 20075 ± 55 ± 32 ± 30.5 ± 0.9
 June/July 20079 ± 80.4 ± 128 ± 3888 ± 17
P. damicornisDecember 2006/March 200712 ± 160.9 ± 22 ± 50.2 ± 0.6
 June/July 200710 ± 160.2 ± 0.524 ± 3191 ± 28
P.rusDecember 2006/March 20073 ± 31 ± 20.3 ± 0.50.5 ± 1
 June/July 20072 ± 21 ± 412 ± 2293 ± 11

In addition, overall detachment was significantly higher in the post-typhoon monitoring sessions (0.58 ± 0.53%) compared with the pre-typhoon period (1.74 ± 2.02%, Wilcoxon signed ranks test; p < 0.005, Tables 2 & 3). This result is the outcome of physical damage to one of the nurseries, where a few trays with Montipora digitata colonies tear away by the waves. Analyzing species-specific post-typhoon coral detachments did not reveal any significant differences (Wilcoxon signed ranks test; p > 0.05, Tables 2 & 3). This outcome indicates nursery construction robustness.

Overall, bleaching was not significantly different in the post- and pre-typhoon periods (Wilcoxon signed ranks test; p > 0.05, Tables 2 & 3). Species-specific analyses revealed significantly higher post-typhoon bleaching values in M. digitata and Pocillopora damicornis (Wilcoxon signed ranks test; p < 0.05, Tables 2 & 3). In general, bleaching is a typical response to stress inflicted during nursery establishment and is evident in higher numbers during the first month after fragments' deployment (Shaish et al. 2008). The only exception is E. lamellosa where bleaching was significantly higher in the pre-typhoon period (Wilcoxon signed Ranks test; p < 0.05, Tables 2 & 3). Partial mortality showed lower levels (< 1%) year round; therefore, data were not included.

Overall pre-typhoon average monthly growth value, 18.7 ± 24.4%, was significantly higher than the post-typhoon values (0.3 ± 15.2%, Wilcoxon signed ranks test; p < 0.001, Tables 2 & 3). The negative effects of the weather on growth rates were further observed in June 2006 values (Table 2). Comparing post-typhoon with pre-typhoon growths, for each species, revealed significantly higher pre-typhoon values for each of the seven species (Wilcoxon signed ranks test; p < 0.001, paired samples test; p < 0.001, Tables 2 & 3). Growth fluctuations were recorded from 1 month to the following, revealed damages inflicted to coral tissues and branch tip breakage from algal removal during routine maintenance, residing fish activities and predation by coralivorous organisms.

Freshwater Seepage Impact on Nursery-Grown Transplants

At the end of August 2006, a month after transplantation was completed, underground freshwater seepage caused turbidity in the seawater at the bottom of the knolls and a decline in salinity (Fig. 2). On the consecutive days, mass mortality of transplants was evident (Fig. 3a–c). It was first revealed by peeling of coral tissue (Fig. 3b), and then, by rapid settlement of turf algae on the bare skeletons (Fig. 3c). We tested salinity levels in nine knolls in sites 2 and 3 several days following the seepage was first noticed and recorded values of 26–28 ppt compared with 30–34 ppt in ambient water. Average mortality at the examined nine knolls was 48 ± 23%, significantly higher compared with the other 27 knolls (7 ± 11%, Mann–Whitney test; p < 0.001, Fig. 3a).


Figure 3. Effects of freshwater seepage at the transplantation site monitored 31 August 2006, 1 month after transplantation, and 2 weeks following the unusual heavy rain (a–c) and bleaching effects on nursery, July 2007 event (d,e). (a) Average mortalities (%) of six different coral species on knolls where low salinity was recorded (solid) and on other knolls in the area (white). (b) A colony of P. damicornis with peeled tissue (17 August 2006). (c) Pocillopora damicornis colony, showing turf algal settlement on bare skeleton (18 August 2006). (d) Bleaching of reared M. digitata corals. (e) Bleaching of reared P. damicornis corals. This figure appears in color in the online version of the article [DOI: 10.1111/j.1526-100X.2009.00647.x].

Download figure to PowerPoint

The coral species were found to differ in their susceptibility to low salinity (Fig. 3a). Montipora digitata was the least sensitive, showing no mortality on the knolls with low salinity and an average mortality of 3 ± 4% on the 11 other knolls. Acropora formosa showed a moderate 8% mortality on the knolls with low salinity and no mortality on the other two knolls. Porites rus and P. damicornis exhibited 42% and 40 ± 21% mortalities in the freshwater seepage area compared with 4 ± 6% and 21 ± 12% mortalities on the other two knolls, respectively. The most susceptible species were M. scabricula and E. lamellosa showing 50 and 75 ± 7% mortality, respectively, in the freshwater seepage area compared with 0 and 2 ± 3% mortality in the two other knolls (Fig. 3a). Due to the low number of repetitions, statistical significance between survivorship at freshwater seepage area versus reference sites was obtained only for E. lamellosa (Mann–Whitney test; p < 0.01).

Southwest Monsoon Impacts on Nursery-Grown Transplants

The 2006 SW monsoon season was extremely tempestuous. Transplants were exposed to the entire monsoon season at their most vulnerable post-transplantation stage (Fig. 2), before an adequate period of acclimation to local conditions. Transplants were monitored for 1 year, once during the typhoon season (November 2006) and three times later (February, May, and July 2007, Table 4; Fig. 2). Mortality and detachment occurred during the entire period whereas partial mortality and bleaching were observed only in the first month post-transplantation (August 2006, minor events) and 1 year later (major bleaching event, July 2007; Table 4; Fig. 4a–c). We compared November 2006 values to the average values of February and May 2007 monitoring sessions in order to define the effects of the SW monsoon season on transplantation, to distinguish from the effects of the fresh-water seepage (August 2006) and the bleaching event (June 2007). Overall percentages of mortality and detachment did not differ significantly between November 2006 and February–May 2007 (paired T test; p > 0.05, Tables 3 & 4). However, site-by-site analyses revealed that November 2006 mortality values were significantly higher in site 2 (paired T test; p < 0.05, Fig. 4a; Tables 3 & 4), and detachment was significantly higher in site 4 (Wilcoxon signed ranks test; p < 0.05, Tables 3 & 4; Fig. 4c). In site 3, no significant difference was recorded between the two periods tested (paired T test; p > 0.05, Tables 3 & 4; Fig. 4b). Analyzing species-specific results revealed that in site 2, mortality in M. digitata was significantly higher in November 2006 compared to February and May 2007 (paired T test; p < 0.05, Tables 3 & 4). In A. formosa, detachment was found to be significantly lower in November 2006 (paired T test; p < 0.05, Tables 3 & 4). In site 3 detachment in E. lamellosa was significantly higher in November 2006 compared to February and May 2007 (paired T Test; p < 0.05, Tables 3 & 4).

Table 4.  Status of transplanted colonies and knolls, 1 year after transplantation; the monitoring of 31 August showed the fresh-water seepage impacts in sites 2 and 3; November monitoring revealed the heavy SW monsoon season and July 2007 monitoring was preformed after a mass bleaching event. “mono” and “poly” refer to combinations of single or several coral species transplanted on a specific knoll.
SpeciesSite No.DateKnolls with Live CoralsAlive ColoniesDetached ColoniesColonies with Partial MortalityBleached Colonies
M. digitata (mono)21 August 065180000
  31 August 06516711396
  November 064772100
  February 07469600
  May 073421700
  July 0732301123
P. damicornis (mono)21 August 069324000
  31 August 0692020197
  November 067373200
  February 07314000
  May 0725000
  July 0711001
M. digitata (poly)21 August 06336000
  31 August 06333140
  November 06317300
  February 07312300
  May 07211000
  July 0728158
P. damicornis (poly)21 August 06336000
  31 August 06332011
  November 0638200
  February 0714100
  May 0713000
  July 0713023
A. formosa (poly)21 August 06336000
  31 August 06329630
  November 06213400
  February 0711400
  May 0700100
  July 0700000
Total for site 2 1 August 0617612000
  31 August 0617463186614
  November 06141526200
  February 07101001400
  May 077611800
  July 0763511835
E. lamellosa (mono)31 August 069324000
  31 August 0692616186
  November 067124500
  February 07117000
  May 0700000
  July 0700000
E. lamellosa (poly)31 August 06336000
  31 August 06326010
  November 06110400
  February 0717000
  May 0711000
  July 0711001
P. rus (poly)31 August 06336000
  31 August 06330050
  November 06327300
  February 07323000
  May 07219000
  July 072190019
M. scabricula (poly)31 August 06336000
  31 August 06330000
  November 06220100
  February 07216300
  May 07212300
  July 072120012
Total for site 3 1 August 0612432000
  31 August 06123476246
  November 06101811300
  February 07463300
  May 07232300
  July 072320032
M. digitata (mono)41 August 064144000
  31 August 0641410307
  November 0641152500
  February 074114000
  May 074112000
  July 07481312381

Figure 4. Cumulative status of transplanted colonies, between August 2006 and July 2007 at different sites: (a) site 2, (b) site 3, and (c) site 4 (only M. digitata). Mortality, gray; detachment, black; partial mortality, hatched; bleaching, white.

Download figure to PowerPoint

No partial mortality or bleaching was observed in any of the knoll during November 2006 (Fig. 4a–c); therefore, no comparison was made with the other monitoring months. Comparing coral mortality in mono- and poly-species knolls (site 2, November 2006) did not reveal any significant difference (one-way analysis of variance [ANOVA]; p > 0.05, Table 4).

Southwest Monsoon Impacts on Nursery

Following the first set of transplantations during October 2006, the nurseries were refurbished with 1,876 new ramets, in addition to the 3,772 colonies remaining from the first year (Fig. 2). The nurseries were monitored four times between October 2006 and July 2007 (Table 5; Fig. 2). The first monitoring was performed during December 2006, and the results were compared with those of March 2007, in order to define the effects of the harsh weather of September until November 2006. Comparing percentages of mortality, detachment, and partial mortality, between December 2006 and March 2007, revealed no significant differences for both the compiled results of all species and for each species individually (Wilcoxon signed ranks test; p > 0.05, paired T test; p > 0.05, Table 5). The effects of the SW monsoon season did not differ between the nursery-grown corals, new transplants (transplanted in October 2006), and the 1-year-old NGCs transplanted in August 2005 (Mann–Whitney; p > 0.05).

Table 5.  Second year nursery; average changes for mortality, detachment, bleaching, and partial mortality of colonies belonging to eight farmed species; the monitoring of July 2007 was preformed after a mass bleaching event.
SpeciesDateMortality (%)Detachment (%)Bleaching (%)Partial Mortality (%)
A. formosaDecember 066.8 ± 3.700.8 ± 0.80.6 ± 0.2
 March 073.4 ± 4.10.7 ± 0.90.2 ± 0.33.7 ± 5.2
 June 071.4 ± 0.6079.5 ± 18.01.0 ± 1.4
 July 0779.8 ± 17.6080.5 ± 27.60
E. lamellosaDecember 062.2 ± 1.72.5 ± 3.22.4 ± 4.60.9 ± 1.4
 March 073.4 ± 5.21.7 ± 1.60.2 ± 0.54.8 ± 9.0
 June 079.4 ± 6.12.2 ± 2.282.6 ± 11.90.7 ± 1.6
 July 079.5 ± 6.70.5 ± 1.174.9 ± 14.343.1 ± 14.7
H.coeruleaDecember 0600.7 ± 1.002.9 ± 4.1
 March 072.6 ± 3.70.7 ± 1.000
 June 077.8 ± 6.94.0 ± 5.600
 July 070013.0 ± 18.40
M. aequituberculataDecember 0611.9 ± 12.701.1 ± 1.52.6 ± 3.7
 March 0715.8 ± 22.3009.0 ± 12.7
 June 0731.6 ± 22.9085.7 ± 8.110.9 ± 15.4
 July 0710.9 ± 15.40100 ± 00
M. digitataDecember 060.2 ± 0.40.1 ± 0.30.2 ± 0.51.4 ± 3.1
 March 070.4 ± 0.70.1 ± 0.100
 June 070.4 ± 0.7000
 July 070.4 ± 0.7098.5 ± 4.10
M. scabriculaDecember 063.7 ± 2.64.1 ± 2.51.0 ± 1.22.7 ± 3.2
 March 076.6 ± 7.25.5 ± 4.201.6 ± 2.1
 June 0710.4 ± 10.70.7 ± 1.487.1 ± 17.58.4 ± 15.8
 July 078.4 ± 6.1088.8 ± 19.048.0 ± 45.9
P. damicornisDecember 0619.1 ± 19.21.5 ± 2.60.4 ± 0.80.7 ± 1.3
 March 074.1 ± 5.60.4 ± 1.102.7 ± 6.3
 June 077.8 ± 10.10.4 ± 0.787.5 ± 33.01.2 ± 3.5
 July 0713.0 ± 21.1089.4 ± 11.746.7 ± 28.7
P. rusDecember 063.0 ± 3.100.6 ± 1.20.3 ± 0.5
 March 072.7 ± 2.12.0 ± 3.30.3 ± 0.90.3 ± 0.6
 June 072.5 ± 2.82.5 ± 5.989.9 ± 14.30.1 ± 0.2
 July 072.4 ± 1.8096.7 ± 3.124.3 ± 26.5
Total nursery valuesDecember
 June 074.80.856.80.8
 July 0716.00.182.322.1

Impacts of Massive Bleaching on Transplantation

High irradiation and elevated seawater temperature during the second half of June 2007 were correlated with a massive bleaching event (Fig. 2), severely affecting transplants in all sites (Table 4; Fig. 4a–c). We compared the July 2007 values with the average values of February and May 2007. Bleaching was not recorded during February and May, whereas in July bleaching peaked to 100% in all sites. Overall percentages of mortality and detachment were significantly higher before the bleaching event (Wilcoxon signed ranks test; p < 0.05, paired sample T-test; p < 0.05, Tables 3 & 4). Analysis per site revealed significant higher mortality before the bleaching event in site 3 only (paired T-test; p < 0.05, Tables 3 & 4). In contrast with these results, percentages of overall partial mortality were significantly higher in July (Wilcoxon signed ranks test; p < 0.05, Tables 3 & 4). Analysis per site revealed significantly higher percentages of colonies with partial mortality in site 2 only (Wilcoxon signed ranks test; p < 0.05, Tables 3 & 4).

Following the bleaching in September 2007, live transplanted colonies were documented in P. rus (n = 9) and M. digitata only (n = 100 colonies, data were not compiled into file).

Impacts of Massive Bleaching on Nursery

The massive bleaching event did not spare the nursery-reared colonies (Table 5, Fig. 3d & 3e). The bleaching effects continued during July 2007 (Table 5). Comparisons were preformed between averages of June and July 2007 to the averages of December 2006 and March 2007 monitoring sessions. Total bleaching and partial mortality were significantly higher during the bleaching months (Wilcoxon signed ranks test; p < 0.001, Tables 3 & 5). Average detachment was significantly lower during the bleaching months (Wilcoxon signed ranks test; p < 0.005, Tables 3 & 5), whereas average mortality did not differ significantly between June and July 2007 to < December 2006 and March 2007 (Wilcoxon signed ranks test; p = 0.05, Tables 3 & 5).

Species-specific values revealed significant differences. Average bleaching was significantly higher during June and July 2007 in seven of the eight species reared in the nursery (Wilcoxon signed ranks test; p < 0.05, Tables 3 & 5), and only in Heliopora coerulea no difference was recorded (Wilcoxon signed ranks test; p > 0.05, Tables 3 & 5). Although, in most species, mortality and partial mortality values were higher in June and July 2007, only in E. lamellosa was the difference significant (Wilcoxon signed ranks test; p < 0.05, Tables 3 & 5). We assume that the non-significant results are due to the high differences recorded between June and July. In M. aequituberculta and M. scabricula, mortality was recorded in June while in A. formosa and P. damicornis mortality increased in July (Table 5). Partial mortality was observed and recorded mainly during July, after the peak of the event. Detachment did not differ significantly in seven of the eight species, except for M. scabricula detachment, where it was significantly higher in December 2006 and March 2007 as compared to June and July 2007. The effect of the bleaching event did not differ between the new transplants (transplanted in October 2006) and the 1-year-old NGCs transplanted in August 2005 (Mann–Whitney; p > 0.05, one-way ANOVA; p > 0.05).


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments

The reef restoration experiments reported here for both nursery farmed and transplants in Bolinao (Philippines) were severely influenced during the 2 years of study, by a forceful southwesterly monsoon season and by stochastic massive environmental events.

The two coral nursery phases in the sheltered area of the Bolinao's large lagoon suffered from two major environmental catastrophes: the 2006 typhoon and the 2007 bleaching events, the latter being the most devastating. In contrast to the other stochastic events, the combined effects of higher water temperatures and irradiation were predictive early warning signals for coral bleaching (Brown 1997; Hoegh-Guldberg 1999; Hughes et al. 2003). Improved nursery management, such as lowering of the nursery bed to deeper water during critical periods to reduce the effects of irradiation and water temperature could have prevented bleaching in nursery-farmed corals, relative to naturally growing shallow water colonies. Susceptibility to bleaching was found to be species-specific. In the nurseries placed at 2-m depth, one (Heliopora coerulea) of the eight species showed resistance to bleaching while partial recovery was observed mainly in Montipora digitata and Porites rus.

Transplantation in this study took place at the beginning of the SW monsoon season, after the summer season. The summer in the Philippines is an unfavorable period for transplantation because of elevated seawater temperatures (Yap 1992; Yap et al. 1998). The transplanted colonies withstood two more stochastic natural disturbance events and a tempestuous southwesterly monsoon season, all potentially affecting survival. The catastrophic event of low salinity resulting from unusually torrential precipitation occurred 1 month after transplantation (August 2006). Similar events had been previously reported on shallow water reefs, with increased sedimentation, nutrients, and reduced light, synergistically affecting mortality (Goreau 1964; Egana & Dislavo 1982; Paerl et al. 1990; Yap et al. 1994; Yap et al. 1994; Larcombe et al. 1996; Porter et al. 1999). Mortality showed species-specific patterns: Echinopora lamellosa, Merulina scabricula, Pocillopora damicornis, and P. rus were considerably affected by the lower salinity whereas M. digitata and Acropora formosa were marginally influenced. The June 2007 mass bleaching was more devastating to transplants. The entire northwest part of the Philippines had been badly affected by bleaching in the 1998 mass-bleaching event (Arceo et al. 2001). During this massive event, Bolinao reefs showed the greatest decrease in live coral cover and were exposed to elevated sea temperature longer than other areas in the Philippines. As in the nurseries, bleaching of transplants showed species-specific patterns (cf. Marshal & Baird 2000; Hughes et al. 2003; McClanahan et al. 2008). Porites rus was more resistant than other species to bleaching. These results are similar to those reported by Yap (2004). The above occurrences emphasize the importance of identifying the most suitable species for restoration in the target site, species with a capability of resisting extreme environmental changes, such as temperature and radiation. Of further importance is the seasonality of transplantation—providing the new transplants an optimal duration for establishment. The most favorable season for transplantation in Bolinao would be January–February, at the end of the NE monsoon season and before the beginning of the summer.

The present bleak situation of coral reefs does not leave much room for an optimistic future, a view supported by the Wakeford et al.'s (2008) conclusion that disturbance intervals shorter than 8 years could reduce the present of dominance of hard coral groups. Furthermore, even commonly occurring natural events such as rainfall and storms may develop to natural catastrophes when their frequency and intensity enhanced (Thibault & Brown 2008).

Many conservation programs and policies focus on a threat-based approach to management of ecosystems (; with an eye to mitigating the most pressing threats to biodiversity. Such conservation planning and action strategy is ineffective and inadequate in areas where unpredictable large-scale natural catastrophes, enhanced by global changes, are occurring frequently. While the persistence of coral reefs depends on the potential for coral communities to respond to climate change, ecological sustainability of impacted reefs cannot seek abatement of most pressing threats to biodiversity anymore. Employing active restoration is becoming an important and inevitable path to reef rehabilitation. Therefore, the assumption that some proportions of habitat goods and services are recoverable through active manipulations, may serve as the best rationale and the best applied tool for mitigating devastating impacts (Rinkevich 2008). Our 2-year follow-up experiments in Bolinao further revealed the significant challenges imposed by natural forces/global changes on planned restoration efforts. They also support suggestions that the current conservation and restoration practices might not be sufficient for forestalling loss of species due to the combination of continuous anthropogenic and worsening climate changes (Hughes et al. 2003; Hoegh-Guldberg et al. 2007). Taking this message further, recent discussions on conservation responses to climate change have offered the option of using dramatic measures, such as the “assisted colonization” approach, suggesting to rescue target species by moving them to sites where they do not currently exist or have not been known to exist in recent history (Hoegh-Guldberg et al. 2008). Whereas the above suggestions may suit a limited number of situations such as conservation of endangered species, they may not be equally suitable to reef restoration as a whole. It is also evident that the current best management tools employed in coral reefs worldwide has failed to achieve conservation objectives, and coral reefs in increasingly documented cases, continue to degrade (Hughes et al. 2003, 2005; Bruno & Selig 2007; Rinkevich 2008).

Responding to the conflicting needs above, we suggest that the establishing of large-scale nurseries and transplantations, together with traditional management tools, are needed to cope with extensive reef degradation on a global scale (Rinkevich 2005, 2006, 2008). With regard to the nursery phase, this study points to the need for depth-flexible structures and for testing species prioritization as pre-site decision. Our results further support the assumption that while it is imperative to considerably revise management protocols and include active reef restoration as an integral part of routine management (Rinkevich 2008), restoring of badly damaged whole reefs is yet an unrealistic aim, given current coral restoration methods and anticipated climate change impacts. Therefore, to generate timely information for management, there is a need for prioritization of the most appropriate and beneficial restoration instruments, developing alternative protocols adapted to specific conditions and circumstances. Parameters such as depth, wave action impacts, substrate composition, and species tolerance, should be carefully evaluated in detailed studies.

Implication for Practice

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments
  • The underwater coral nursery is an approved practical instrument to farm large numbers of coral colonies from a variety of species, preceding their transplantation into denuded reefs. The nurseries constructed for this study withstood rough weather conditions, attesting to their long-term use. Improving the nursery construction to fit environmental changes will enhance survivorship rates of farmed colonies.
  • Corals revealed species-specific tolerance and growth capabilities under different environmental stressors. Of the seven species used in this study, two exhibited high tolerance to low salinity and bleaching. Restoration acts should consider negative impacts of unpredictable harsh weather. Taking into account the use of species combination is an advisable management instrument for the successes of restoration.
  • Global climatic changes are expected to impose ever-increasing challenges on future restoration measures. However, it is our view that extensive reef degradation on a global scale can only be counteracted by establishing large-scale nurseries and transplantation acts, together with traditional management tools.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments

This study is part of the Ph.D. dissertation research by L. Shaish and was supported by grants from the World Bank/GEF and INCO-DEV (REEFRES-510657) projects. We thank the people in Bolinao Marine Laboratory for their help and hospitality.


  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Implication for Practice
  8. Acknowledgments
  • Allison, G. W., S. D. Gaines, J. Lubchenco, and H. P. Possingham. 2003. Ensuring persistence of marine reserves catastrophes require adopting an insurance actor. Ecological Applications 13:S8S24.
  • Arceo, H. O., M. C. Quibilan, P. M. Alino, G. Lim, and W. Y. Licuanan. 2001. Coral bleaching in Philippine reefs: coincident evidences with mesoscale thermal anomalies. Bulletin of Marine Science 29:579593.
  • Baskett, M. L., S. D. Gaines, and R. M. Nisbet. 2009. Symbiont diversity may help coral reefs survive moderate climate change. Ecological Applications 19:317.
  • Brown, B. E. 1997. Coral bleaching: causes and consequences. Coral Reef 16:129138.
  • Bruno, J. F., and E. R. Selig. 2007. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. PLoS ONE 2:e711.
  • Chadwick-Furman, N. E. 1996. Reef coral diversity and global change. Global Change Biology 2:559568.
  • Diego-McGlone, M. L. S., R. V. Azanza, C. L. Villanoy, and G. S. Jacinto. 2008. Eutrophic waters, algal bloom and fish kill in fish farming areas in Bolinao, Pangasinan, Philippines. Marine Pollution Bulletin 57:295301.
  • Done, T. J. 1992. Constancy and change in some Great Barrier Reef coral communities: 1980–1990. American Zoologist 32:655662.
  • Easterling, D. R., G. A. Meehl, C. Parmesan, S. A. Changnon, T. R. Karl, and L. O. Mearns. 2000. Climate extremes: observations, modeling, and impacts. Science 289:20682074.
  • Egana, A. C., and L. H. DiSalvo. 1982. Mass expulsion of zooxanthellae by Easter Island corals. Pacific Science 36:6163.
  • Epstein, N., R. P. M. Bak, and B. Rinkevich. 2001. Strategies for gardening denuded coral reef areas: the applicability of using different types of coral material for reef restoration. Restoration Ecology 9:432442.
  • Folke, C., S. Carpenter, B. Walker, M. Scheffer, T. Elmqvist, L. Gunderson, and C. S. Holling. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics 35:557581.
  • Game, E. T., M. E. Watts, S. Wooldridge, and H. P. Possingham. 2008. Planning for persistence in marine reserves: a question of catastrophic importance. Ecological Applications 18:670680.
  • Gomez, E. D. 1997. Reef management in developing countries: a case study in the Philippines. Coral Reefs 16:S3S8.
  • Gomez, E. D. 2001. Is the degradation of resources in the South China Sea reversible? Approaches to sustainable management. International Symposium on Protection and Management of Coastal Marine Ecosystem. 195204 EAS/RCU, UNEP, Bangkok.
  • Goreau, T. F. 1964. Mass expulsion of zooxanthellae from Jamaican reef communities after hurricane Flora. Science 145:383386.
  • Grigg, R. W., and S. J. Dollar. 1990. Natural and anthropogenic disturbance on coral reefs. Pages 439452 in In: Coral reefs. Vol. 25. Ecosystems of the world. Elsevier, Amsterdam.
  • Halford, A., A. J. Chael, D. Ryan, and D. M. C. B. Williams. 2004. Resilience to large-scale disturbance in coral and fish assemblages on the Great Barrier Reef. Ecology 85:18921905.
  • Hodgson, G. 1999. A global assessment of human effects on coral reefs. Marine Pollution Bulletin 38:345355.
  • Hoegh-Guldberg, O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50:839866.
  • Hoegh-Guldberg, O., and G. J. Smith. 1989. The effect of sudden changes in temperature, irradiance and salinity on the population density and export of zooxanthellae from the reef corals Stylophora pistillata (Esper 1797) and Seriatopora hystrix (Dana 1846). Journal of Experimental Marine Biology and Ecology 129:279303.
  • Hoegh-Guldberg O., P. J. Mumby, A. J. Hoote, R. S. Steneck, P. Greenfield, E. Gomez, et al. 2007. Coral reefs under rapid climate change and ocean acidification. Science 318:17371742.
  • Hoegh-Guldberg, O., L. Hughes, S. McIntyre, D. B. Lindenmayer, C. Parmesan, H. P. Possingham, and C. D. Thomas. 2008. Assisted colonization and rapid climate change. Science 321:345346.
  • Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S. Connolly, C. Folke, et al. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929933.
  • Hughes, T. P., D. R. Bellwood, C. Folke, R. S. Steneck, and J. Wilson. 2005. New paradigms for supporting the resilience of marine ecosystems. Trends in Ecology and Evolution 20:380386.
  • Jackson, J. B. C., M. X. Kirby, W. H. Berger, K. A. Bjorndal, L. W. Botsford, B. J. Bourque, et al. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629638.
  • Larcombe, P., K. Woolfe, and R. Purdon. 1996. Great barrier reef: terrigenous sediment flux and human impacts. James Cook University, Townsville.
  • McClanahan, T. R., M. Ateweberhan, and J. Omukoto. 2008. Long-term changes in coral colony size distributions on Kenyan reefs under different management regimes and across the 1998 bleaching event. Marine Biology 153:755768.
  • Manning, A. D., D. B. Lindenmayer, and J. Fischer. 2006. Stretch goals and backcasting: approaches for overcoming barriers to large-scale ecological restoration. Restoration Ecology 14:487492.
  • Marshall, P. A., and A. H. Baird. 2000. Bleaching of corals on the Great Barrier Reef: differential susceptibilities among taxa. Coral Reefs 19:155163.
  • Moberg, F., and C. Folke 1999. Ecological goods and services of coral reef ecosystems. Ecological Economics 29:215233.
  • Mumby, P. G., and R. S. Steneck. 2008. Coral reef management and conservation in light of rapidly evolving ecological paradigm. Trends in Ecological and Evolution 23:555563.
  • Paerl, H. W., J. Rudek, and M. A. Mallin. 1990. Stimulation of phytoplankton production in coastal waters by natural rainfall inputs: nutritional and trophic implications. Marine Biology 107:247254.
  • Pittock, A. B. 1999. Coral Reef and environmental changes: adaptation to what? American Zoologist 39:1029.
  • Porter J. W., S. K. Lewis, and K. G. Porter. 1999. The effect of multiple stressors on the Florida Keys coral reef ecosystem: a landscape hypothesis and a physiological test. Limnology and Oceanography 44:941949.
  • Puotinen, M. L. 2007. Modeling the risk of cyclone wave damage to coral reef using GIS: a case study of the Grate Barrier Reef, 1969–2003. International Journal of Geographical Information Science 21:97120.
  • Putchim, L., N. Thongtham, A. Hewett, and H. Chansang. 2008. Survival and growth of Acropora spp. in mid-water nursery and after transplantation at Phi Phi Islands, the Andaman Sea, Thailand. Proceeding of the 11th International Coral Reef Symposium, Florida, Session number 24:12581261.
  • Raymundo, L. J., A. P. Maypa, E. D. Gomez, and P. Cadiz. 2007. Can dynamite-blasted reefs recover? A novel, low-tech approach to stimulating natural recovery in fish and coral populations. Marine Pollution Bulletin 54:10091019.
  • Rinkevich, B. 1995. Restoration strategies for coral reefs damaged by recreational activities: the use of sexual and asexual recruits. Restoration Ecology 3:241.
  • Rinkevich, B. 2000. Steps towards the evaluation of coral reef restoration by using small branch fragments. Marine Biology 136:807812.
  • Rinkevich, B. 2005. Conservation of coral reefs through active restoration measures: recent approaches and last decade progress. Environmental Science & Technology 39:43334342.
  • Rinkevich, B. 2006. The coral gardening concept and the use of underwater nurseries; lesson learned from silvics and silviculture. Pages 291–301 in W. P.Precht, editor. Coral Reef Restoration Handbook. CRC Press, Boca Raton, Florida.
  • Rinkevich, B. 2008. Management of coral reefs: we have gone wrong when neglecting active reef restoration. Marine Pollution Bulletin 56:18211824.
  • Scheffer, M., S. R. Carpenter, J. A. Foley, C. Folke, and B. Walker. 2001. Catastrophic shifts in ecosystems. Nature 413:591596.
  • Shafir, S., J. Van Rijn, and B. Rinkevich. 2006a. Steps in the construction of underwater coral nursery, an essential component in reef restoration acts. Marine Biology 149:679687.
  • Shafir, S., J. Van Rijn, and B. Rinkevich. 2006b. A mid-water coral nursery. Proceeding of the 10th International Coral Reef Symposium, Okinawa, Japan, 16741679.
  • Shaish, L., G. Levy, E. Gomez, and B. Rinkevich. 2008. Fixed and suspended coral nurseries in the Philippines: establishing the first step in the “gardening concept” of reef restoration. Journal of Experimental Marine Biology and Ecology 358:8697.
  • Soong, K., and T. Chen. 2003. Coral transplantation: regeneration and growth of Acropora fragments in a nursery. Restoration Ecology 11: 6271.
  • Thibault, K. M., and J. H. Brown. 2008. Impact of an extreme climatic event on community assembly. Proceedings of the National Academy of Science, USA 105:34103415.
  • Underwood, A. J. 1981. Techniques of analysis of variance in experimental marine biology and ecology. Oceanography and Marine Biology Annual Review 19:513605.
  • Wakeford, M., T. J. Done, and C. R. Johnson. 2008. Decadal trends in a coral community and evidence of changed disturbance regime. Coral Reefs 27:113.
  • Wilkinson, C. 2002. Status of coral reefs of the world. Australian Institute of Marine Science Townsville, Australia.
  • Yap, H. T. 1992. Marine environmental problems experiences of developing regions. Marine Pollution Bulleting 25:3740.
  • Yap, H. T. 2003. Coral reef “restoration” and coral transplantation. Marine Pollution Bulletin 46:529.
  • Yap, H. T. 2004. Different survival of coral transplants on various substrates under elevated water temperatures. Marine Pollution Bulletin 49:306312.
  • Yap, H. T., R. M. Alvarez, H. M. Custodio, and R. M. Dizon. 1998. Physiological and ecological aspects of coral transplantation. Journal of Experimental Marine Biology and Ecology 229:6984.
  • Yap, H. T., A. R. F. Montebon, and R. M. Dion. 1994. Energy flow and seasonality in tropical coral reef flat. Marine Ecology Progress Series 103:3543.