Closing the circle: is it feasible to rehabilitate reefs with sexually propagated corals?

Sexual propagation of corals specifically for reef rehabilitation remains largely experimental. In this study, we refined low technology culture and transplantation approaches and assessed the role of colony size and age, at time of transfer from nursery to reef, on subsequent survival. Larvae from Acropora millepora were reared from gametes and settled on engineered substrates, called coral plug-ins, that were designed to simplify transplantation to areas of degraded reef. Plug-ins, with laboratory spawned and settled coral recruits attached, were maintained in nurseries until they were at least 7 months old before being transplanted to replicate coral limestone outcrops within a marine protected area until they were 31 months old. Survival rates of transplanted corals that remained at the protected in situ nursery the longest were 3.9–5.6 times higher than corals transplanted to the reef earlier, demonstrating that an intermediate ocean nursery stage is critical in the sexual propagation of corals for reef rehabilitation. 3 years post-settlement, colonies were reproductively mature, making this one of few published studies to date to rear a broadcasting scleractinian from eggs to spawning adults. While our data show that it is technically feasible to transplant sexually propagated corals and rear them until maturity, producing a single 2.5-year-old coral on the reef cost at least US$60. ‘What if’ scenarios indicate that the cost per transplantable coral could be reduced by almost 80 %, nevertheless, it is likely that the high cost per coral using sexual propagation methods would constrain delivery of new corals to relatively small scales in many countries with coral reefs.     

Coral Reef Restoration (Bolinao,Philippines) in the Face of Frequent Natural Catastrophes

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.     

Fixed and suspended coral nurseries in the Philippines: Establishing the first step in the “gardening concept” of reef restoration

The worldwide degradation of reef ecosystems has promoted the advocators of restoration acts to the foreground. Here, we describe the results of the first step of large-scale restoration based on the “gardening with corals” concept. During June-September 2005, two coral nurseries were established in Bolinao, the Philippines, in front of Silaqui Island, in a shallow (2 m depth) sandy lagoon. Two types of nurseries were employed: (1) suspended nursery; (2) leg-fixed nursery. The nursery held a total number of 6824 ramets, from seven coral species representing different growth forms (branching, leaf-like and sub-massive forms) and different growth rates (fast and slow growing species). Each species was represented by several genotypes. During one year, we analyzed and compared survivorship, bleaching and growth rates of fragments between the different nurseries, species and genotypes. Survivorship, which was high in both nurseries, > 85%, fluctuated between the different species indicating that different species require different rearing methodologies. Mortality and detachment was subjected to environmental conditions, especially affected by the typhoons prevailing in this part of the world. The one-year nursery phase produced sizeable colonies, especially of branching forms, suitable for transplantation.     

Mid-water rope nursery—Testing design and performance of a novel reef restoration instrument

Fast degradation of coral reefs worldwide has promoted the exploitation of active restoration instruments, one of which is the ‘gardening concept’. This concept comprises two phases: (1) establishing in situ coral nurseries for rearing large numbers of coral fragments; (2) their transplantation onto denuded reefs. This study tested the design and performance of a novel mid-water floating nursery instrument, a ‘rope nursery’. This nursery accommodated small coral fragments attached to a rope, creating an easily constructed nursery bed that is rapid and inexpensive. Two sets of experiments were conducted: the first tested two mid-water rope nursery prototypes in small-scale trials that tested depth, coral genotypes and construction stability, whereas the second set incorporated lessons learned from the first set, and was designed to carry larger numbers of colonies. These highly economical nurseries (US$ 0.11/fragment) revealed high survivorship low detachment and fast growth rates compared to previous coral-nursery types. Moreover, the coiling force of the ropes adequately held fragments without adhesives, and the minimal surface area of rope nursery beds provided not only improved water flux around farmed corals, but also reduced proliferation of fouling organisms. The rope nursery prototypes studied here attest to the diversity of their potential uses under various conditions and demands, making the construction of large scale nurseries a very feasible target. This restoration instrument was proven to be an effective coral reef rehabilitation tool.     

Testing the first phase of the ‘gardening concept’ as an applicable tool in restoring denuded reefs in Tanzania

Studies on coral reef restoration through a two-step coral gardening protocol have lately proved it to be a viable solution for future reef restoration. This involves a first step of gardening small colonies in mid-water nurseries and a second step, their transplantation, upon reaching suitable size, onto the pre-surveyed damaged areas. We established in September 2007 two mid-water nurseries, each holding 10,000 fragments measuring 2 cm average initial size, at 4 m depths (high tide) in Zanzibar and Mafia Islands, Tanzania. Each nursery comprised six species, each of which was represented by three genotypes. During 9 months, we followed developments by analyzing and comparing survivorship and growth rates of fragments between the different nurseries, species and genotypes. A significant difference between species survival and growth rates was observed in acroporid species, in Pocillopora verrucosa and Millepora sp., which showed better success than Porites cylindrica. In both sites, Millepora suffered no mortality and other species exhibited low mortality, ranging (per coral genotype) between 3% and 24% in Zanzibar (most cases below 10%) and between 13% and 44% (mostly below 25%) in Mafia Island. Most of fragments’ mortality occurred during the first two nursery months. Coral species in Zanzibar nursery also performed better in growth rates than those in Mafia, but in both sites, farmed corals were ready for transplantation just 9 months after the nursery was set up. Economic evaluations involved in the overall nursery set-up and the results indicated that the coral gardening approach could be used in Tanzania to generate large quantities of coral colonies for the restoration of damaged reefs at relatively low cost.     

Long-term heightened larval production in nursery-bred coral transplants

The ‘gardening coral reefs’ method is part of the approaches proposed for counteracting the substantial impacts of global climate change on the survival of coral reefs. It incorporates ecosystem engineering strategies for coral nursery farming and coral colonies out-planting. This study explores the reproductive output of three sets of nursery-grown Stylophora pistillata colonies along eight reproductive seasons following transplantation, as compared to that of native corals. When native and transplanted corals grew side by side in a disturbed environment, the nursery-grown transplants showed enhanced larval release (2.6–22.5 times more planulae/colony; multiyear average: 11.6±1.8 planulae/transplant vs. 1.5±0.3 planulae/native colony) with higher percentages of gravid colonies (91±2.1% transplants vs. 34±7.6% native colonies). The inherently enhanced larval production of transplants, maintained for such a long period of time post-transplantation, reveals a possible enduring impact of the nursery conditions on future fitness and ecological traits of transplants. This is further supported by the emerging documentation regarding the enhanced growth of corals under nursery conditions, which continues to be detected even years after transplantation was conducted on the natural reef. The above enhancement of coral reproduction can be harnessed as a human intervention tool for countering global climate change impacts.     

Effects of intermittent flow and irradiance level on back reef Porites corals at elevated seawater temperatures

Corals inhabiting shallow back reef habitats are often simultaneously exposed to elevated seawater temperatures and high irradiance levels, conditions known to cause coral bleaching. Water flow in many tropical back reef systems is tidally influenced, resulting in semi-diurnal or diurnal flow patterns. Controlled experiments were conducted to test effects of semi-diurnally intermittent water flow on photoinhibition and bleaching of the corals Porites lobata and P. cylindrica kept at elevated seawater temperatures and different irradiance levels. All coral colonies were collected from a shallow back reef pool on Ofu Island, American Samoa. In the high irradiance experiments, photoinhibition and bleaching were less for both species in the intermittent high-low flow treatment than in the constant low flow treatment. In the low irradiance experiments, there were no differences in photoinhibition or bleaching for either species between the flow treatments, despite continuously elevated seawater temperatures. These results suggest that intermittent flow associated with semi-diurnal tides, and low irradiances caused by turbidity or shading, may reduce photoinhibition and bleaching of back reef corals during warming events.     

Differential nitric oxide synthesis and host apoptotic events correlate with bleaching susceptibility in reef corals

Coral bleaching poses a threat to coral reefs worldwide. As a consequence of the temperature-induced breakdown in coral–dinoflagellate symbiosis, bleaching can have extensive effects on reef communities. However, our understanding of bleaching at a cellular level is limited, and this is particularly true regarding differential susceptibility among coral species. Recent work suggests that bleaching may represent a host innate immune-like response to symbiont dysfunction that involves synthesis of the signalling compound nitric oxide (NO) and the induction of host apoptotic-like cell death. In this study, we examined the activity of apoptosis-regulating enzymes alongside oxidised NO accumulation (a proxy for NO synthesis) in the reef corals Acropora millepora, Montipora digitata, and Pocillopora damicornis during experimental thermal stress. P. damicornis was the most sensitive species, suffering mortality (tissue sloughing) after 5 days at 33 °C but non-lethal bleaching after 9 days at 31.5 °C. A. millepora bleached at 33 °C but remained structurally intact, while M. digitata showed little evidence of bleaching. P. damicornis and A. millepora both exhibited evidence of temperature-induced NO synthesis and, after 5 days of heating, levels of oxidised NO in both species were fivefold higher than in controls maintained at 28.5 °C. These responses preceded bleaching by a number of days and may have occurred before symbiont dysfunction (measured as chlorophyll a degradation and oxidised NO accumulation). In A. millepora, apparent NO synthesis correlated with the induction of host apoptotic-like pathways, while in P. damicornis, the upregulation of apoptotic pathways occurred later. No evidence of elevated NO production or apoptosis was observed in M. digitata at 33 °C and baseline activity of apoptosis-regulating enzymes was negligible in this species. These findings provide important physiological data in the context of the responses of corals to global change and suggest that early events in the host may be important in the collapse of the coral–dinoflagellate symbiosis.     

Effects of coral bleaching on the feeding response of two species of coral-feeding fish

Coral bleaching is an increasingly prominent threat to coral reef ecosystems, not only to corals, but also to the many organisms that rely on coral for food and shelter. Coral-feeding fishes are negatively affected by coral loss caused by extensive bleaching, but it is unknown how feeding behaviour of most corallivorous fishes changes in response to coral bleaching. In this study, coral bleaching was experimentally induced in situ to examine the feeding response of two obligate corallivorous fish, Labrichthys unilineatus (Labridae) and Chaetodon baronessa (Chaetodontidae). Feeding rates were monitored before, during, and immediately after experimental bleaching of prey corals. L. unilineatus significantly increased its feeding on impacted corals during bleaching, but showed a steady decline in feeding once corals were fully bleached. Feeding response of L. unilineatus appears to parallel the expected stress-induced mucous production by bleaching colonies. In contrast, C. baronessa preferentially fed from healthy colonies over bleached colonies, although bleached colonies were consumed for five days following manipulation. Feeding by corallivorous fishes can play an important role in determining coral condition and mortality of corals following stress induced bleaching.     

Severity of the 1998 and 2005 bleaching events in Venezuela, southern Caribbean

This study describes the severity of the 2005 bleaching event at 15 reef sites across Venezuela and compares the 1998 and 2005 bleaching events at one of them. During August and September 2005, bleached corals were first observed on oceanic reefs rather than coastal reefs, affecting 1 to 4% of coral colonies in the community (3 reef sites, n = 736 colonies). At that time, however, no bleached corals were recorded along the eastern coast of Venezuela, an area of seasonal upwelling (3 reefs, n = 181 colonies). On coastal reefs, bleaching started in October but highest levels were reached in November 2005 and January 2006, when 16% of corals were affected among a wide range of taxa (e.g. scleractinians, octocorals, Millepora and zoanthids). In the Acropora habitats of Los Roques (an oceanic reef),no bleached was recorded in 2005 (four sites,n = 643 colonies). At Cayo Sombrero, a coastal reef site, bleaching was less severe in 1998 than in 2005 (9% of the coral colonies involving 2 species vs. 26% involving 23 species, respectively). Our results indicate that bleaching was more severe in 2005 than in 1998 on Venezuelan reefs; however, no mass mortality was observed in either of these two events.     

Changes in Bleaching Susceptibility among Corals Subject to Ocean Warming and Recurrent Bleaching in Moorea,French Polynesia

Background

Climate-induced coral bleaching poses a major threat to coral reef ecosystems, mostly because of the sensitivities of key habitat-forming corals to increasing temperature. However, susceptibility to bleaching varies greatly among coral genera and there are likely to be major changes in the relative abundance of different corals, even if the wholesale loss of corals does not occur for several decades. Here we document variation in bleaching susceptibility among key genera of reef-building corals in Moorea, French Polynesia, and compare bleaching incidence during mass-bleaching events documented in 1991, 1994, 2002 and 2007.

Methodology/Principal Findings

This study compared the proportion of colonies that bleached for four major genera of reef-building corals (Acropora, Montipora, Pocillopora and Porites), during each of four well-documented bleaching events from 1991 to 2007. Acropora and Montipora consistently bleached in far greater proportions (up to 98%) than Pocillopora and Porites. However, there was an apparent and sustained decline in the proportion of colonies that bleached during successive bleaching events, especially for Acropora and Montipora. In 2007, only 77% of Acropora colonies bleached compared with 98% in 1991. Temporal variation in the proportion of coral colonies bleached may be attributable to differences in environmental conditions among years. Alternately, the sustained declines in bleaching incidence among highly susceptible corals may be indicative of acclimation or adaptation.

Conclusions/Significance

Coral genera that are highly susceptible to coral bleaching, and especially Acropora and Montipora, exhibit temporal declines in their susceptibility to thermal anomalies at Moorea, French Polynesia. One possible explanation for these findings is that gradual removal of highly susceptible genotypes (through selective mortality of individuals, populations, and/or species) is producing a coral assemblage that is more resistant to sustained and ongoing ocean warming.     

Life histories predict coral community disassembly under multiple stressors

Climate change is reshaping biological communities against a background of existing human pressure. Evaluating the impacts of multiple stressors on community dynamics can be particularly challenging in species‐rich ecosystems, such as coral reefs. Here, we investigate whether life‐history strategies and cotolerance to different stressors can predict community responses to fishing and temperature‐driven bleaching using a 20‐year time series of coral assemblages in Kenya. We found that the initial life‐history composition of coral taxa largely determined the impacts of bleaching and coral loss. Prior to the 1998 bleaching event, coral assemblages within no‐take marine reserves were composed of three distinct life histories – competitive, stress‐tolerant and weedy– and exhibited strong declines following bleaching with limited subsequent recovery. In contrast, fished reefs had lower coral cover, fewer genera and were composed of stress‐tolerant and weedy corals that were less affected by bleaching over the long term. Despite these general patterns, we found limited evidence for cotolerance as coral genera and life histories were variable in their sensitivities to fishing and bleaching. Overall, fishing and bleaching have reduced coral diversity and led to altered coral communities of ‘survivor’ species with stress‐tolerant and weedy life histories. Our findings are consistent with expectations that climate change interacting with existing human pressure will result in the loss of coral diversity and critical reef habitat.     

Macroalgae reduces survival of nursery‐reared Acropora corals in the Florida reef tract

Recent declines in coral populations along the Florida reef tract have prompted the establishment of coral restoration programs which raise coral species, such as the threatened Acropora cervicornis, in nurseries ready for outplanting. Large numbers of nursery‐reared coral colonies have been outplanted along the Florida reef tract in recent years, yet few studies have characterized benthic habitats that are considered optimal for colony survival. In 2016, we surveyed 23 A. cervicornis restoration sites, located at six different reefs in the upper Florida Keys. We examined the condition of the outplanted corals and quantified the benthic assemblages adjacent to the outplanted coral colonies. We found that where A. cervicornis survived for more than 1 year, the substrate significantly supported less brown macroalgae of the genus Dictyota than at sites where A. cervicornis had died. Coral survival was highest at sites with less than 15% Dictyota cover. These results suggest that the habitat conditions that supported Dictyota spp. were not conducive to A. cervicornis growth and survival. Restoration practitioners should avoid attaching nursery‐raised corals to substrate with Dictyota spp. cover greater than 15%.     

Relocating bleached Platygyra sinensis facilitates recovery from thermal stress during a minor bleaching event

The recovery of bleached corals is crucial in ensuring the persistence of the coral reef ecosystem function. This study investigated whether relocating bleached Platygyra sinensis colonies was a viable measure to accelerate their recovery. During a mild bleaching event in 2014, eight bleached colonies of P. sinensis were relocated from an affected reef at Sultan Shoal, Singapore, to a reef at Kusu that was less impacted. Another eight colonies at Sultan Shoal were tagged as controls. After five months, 88% of relocated bleached colonies at Kusu showed full recovery whereas only 25% of the control bleached colonies at Sultan Shoal had recovered. The differential coral recovery among the two sites was most likely due to lower seawater temperatures and faster water flow at Kusu, which helped to mitigate the effects of thermal stress on the bleached corals. This relocation study demonstrated that relocating bleached P. sinensis to sites with more favourable environmental conditions is a viable approach to reduce bleaching impacts for this species.     

Evolution of fringing reefs: space and time constraints from the Gulf of Aqaba

This study documents the pattern and rate of reef growth during the late Holocene as revealed by unique geological conditions at the subsiding NW Gulf of Aqaba. We discovered that the modern fringing reef near the city Elat grows on top of a fossil submerged mid-Holocene reef platform. Four coral cores from the fossil platform were dated using the radiocarbon and U-Th methods. The fossil corals range from 5.6±0.1 to 2.4±0.03 ka, constraining the initiation of the modern reef to 2,400 years ago at most. We documented the detailed morphology of the reef using aerial photographs and scuba diving. The survey shows that at its northern end, growth of the 2-km-long reef is inhibited by an active alluvial fan, and it is composed of isolated knolls that are just approaching the sea surface. Towards the south, the knolls are progressively larger and closer together, until they form a continuous reef platform. Along this north-to-south trend we follow the evolution of reef morphology, changes in coral distribution, and the development of a lagoon separated from the open sea. Based on these observations, we suggest a four-stage reef growth model: (a) the reef initiates as coral colonies, forms knolls, and begins to grow upward, limited by the sea surface. (b) Upon reaching the surface, the knolls spread laterally, preferentially parallel to the dominant wave direction assuming an elongated morphology. (c) Continued growth results in adjacent knolls eventually coalescing to form a continuous jagged reef. We interpret the spurs-and-grooves morphology that can be traced across the reef at Elat as remnants of the original trends of knolls. (d) While reef expansion continues, the original knoll trends may be obscured as a massive reef front takes shape. Considering reef growth rates and observations from the modern reef at Elat, this evolution scheme predicts an age range of 10³ years for corals on the reef platform. The range and distribution of radiometric ages we obtained from the fossil reef platform underlying the living Elat reef confirm this hypothesis.     

Engineering of coral reef larval supply through transplantation of nursery-farmed gravid colonies

The continuous worldwide degradation of coral reefs raises an urgent need for novel active restoration techniques as traditional conservation practices have failed to impede the incessant reefs' decline. While applying the “gardening coral reefs” methodology in Eilat (Red Sea, Israel), we examined reproductive outputs of naturally-grown and outplanted, nursery-farmed Stylophora pistillata colonies from three coral-transplantation trials (November 2005, May 2007, and September 2008), along three reproductive seasons. Surprisingly, transplanted colonies showed better reproductive capacities than the natal Stylophora colonies during > 4 post-transplantation years. A higher percentage of nursery-farmed colonies released planula larvae as compared to naturally-grown colonies. Gravid transplants also shed more planulae per colony, yielding significantly augmented numbers of total planulae over naturally developed S. pistillata colonies. Our results indicate that nursery-grown corals may be used to enhance reef resilience by contributing to the larval pool, forming an engineered larval dispersal instrument for reef rehabilitation.     

The transformation of Caribbean coral communities since humans

The mass die‐off of Caribbean corals has transformed many of this region’s reefs to macroalgal‐dominated habitats since systematic monitoring began in the 1970s. Although attributed to a combination of local and global human stressors, the lack of long‐term data on Caribbean reef coral communities has prevented a clear understanding of the causes and consequences of coral declines. We integrated paleoecological, historical, and modern survey data to track the occurrence of major coral species and life‐history groups throughout the Caribbean from the prehuman period to the present. The regional loss of Acropora corals beginning by the 1960s from local human disturbances resulted in increases in the occurrence of formerly subdominant stress‐tolerant and weedy scleractinian corals and the competitive hydrozoan Millepora beginning in the 1970s and 1980s. These transformations have resulted in the homogenization of coral communities within individual countries. However, increases in stress‐tolerant and weedy corals have slowed or reversed since the 1980s and 1990s in tandem with intensified coral bleaching and disease. These patterns reveal the long history of increasingly stressful environmental conditions on Caribbean reefs that began with widespread local human disturbances and have recently culminated in the combined effects of local and global change.     

Consequences of fission in the coral <Emphasis Type="Italic">Siderastrea siderea</Emphasis>: growth rates of small colonies and clonal input to population structure

Colony age and size can be poorly related in scleractinian corals if colonies undergo fission to form smaller independent patches of living tissue (i.e., ramets), but the implications of this life-history characteristic are unclear. This study explored the ecological consequences of the potential discrepancy between size and age for a massive scleractinian, first by testing the effect of colony origin on the growth of small colonies, and second by quantifying the contribution of ramets to population structure. Using Siderastrea siderea in St. John (US Virgin Islands) as an experimental system, the analyses demonstrated that the growth of small colonies derived from sexual reproduction was 2.5-fold greater than that of small ramets which were estimated to be ≈100 years older based on the age of the parent colonies from which they split. Although fission can generate discrete colonies, which in the case of the study reef accounted for 42% of all colonies, it may depress colony success and reef accretion through lowered colony growth rates.     

Improved sustainable maintenance for mid-water coral nursery by the application of an anti-fouling agent

The ‘gardening concept’ for reef restoration focuses on coral colonies farming in mid-water nurseries before their transplantation onto denuded reef areas. Nurseries situated in a nutrient-enriched environment significantly curtail nursery time, but extend labor, as nursery construction and farmed corals must be frequently cleaned from competing fouling organisms. Mass farming of corals calls, therefore, for efficient and cheap maintenance methodologies, which we here tested by employing Aqua-guard M250, an anti-fouling agent used in the fish farming industry. We found that this anti-fouling paint, while reducing fouling organisms on nursery components during the crucial phase of coral ramets' development from nubbins and small fragments sizes to colony sizes suitable for transplantation, is not toxic to maricultured coral fragments that staged more than 2 cm away from the paint. Applying small quantities of such antifouling paint to coral nurseries, while restricting its use to nursery components that are not in direct contact with farmed coral material, reduces fouling coverage and cleaning procedures by 90%.     

The role of in situ coral nurseries in supporting mobile invertebrate epifauna

Coral nurseries are commonly employed to generate coral material for reef restoration projects, but observations of epifaunal organisms utilising the nurseries for food and shelter indicate that they can also provide important functions beyond that of coral propagation. To examine the level of biodiversity that can be supported by coral nurseries, and investigate if epifaunal communities were influenced by the presence of live coral tissue, we compared the abundance, diversity and community composition of mobile invertebrate epifauna associated with live and dead fragments of three coral species (Pocillopora acuta, Echinopora lamellosa, Platygyra sinensis) that were reared in an in situ nursery. A total of 418 mobile invertebrates spanning 63 taxa were recorded from 22 coral colonies. The three coral species hosted significantly different epifaunal communities, most likely a consequence of the difference in growth forms of the coral hosts. Significant differences in epifaunal communities were only observed between live and dead colonies of P. acuta, indicating that resource provisioning in this species is particularly influenced by the presence of live tissue. Our findings showed that coral nurseries can support a range of mobile invertebrates and function as tools to conserve threatened mobile invertebrates. This ecological function is under-studied and should be assessed in restoration programs for the conservation of corals and associated fauna.