In situ nurseries enhance coral transplant growth in sedimented waters

In situ nurseries have been a crucial part of coral reef restoration initiatives for the past two decades. However, the advantages over direct transplantation in sedimented waters has yet to be examined. In the present study, we showed that Pachyseris speciosa and Pocillopora damicornis fragments reared in in situ nurseries (NR) in Singapore’s sedimented waters grew significantly faster (by three to five times) than those which were directly transplanted (DT) onto the substrates. The increased growth rate during the nursery phase augmented the size of NR transplants, and had a flow-on effect on their performance during the post-transplantation phase. Overall, the maximum diameter of the NR transplants was 1.8–2.7 times larger than DT transplants after 11 months. The growth enhancement of the nursery-reared transplants improved the cost-effectiveness of our restoration effort: the estimated cost per centimetre growth of NR transplants was one-fifth of the DT corals despite the additional costs incurred to construct the nurseries. These results highlight that coral nurseries are beneficial to reef restoration in chronically sedimented waters.     

Differential survival of nursery‐reared Acropora cervicornis outplants along the Florida reef tract

In recent decades, the Florida reef tract has lost over 95% of its coral cover. Although isolated coral assemblages persist, coral restoration programs are attempting to recover local coral populations. Listed as threatened under the Endangered Species Act, Acropora cervicornis is the most widely targeted coral species for restoration in Florida. Yet strategies are still maturing to enhance the survival of nursery‐reared outplants of A. cervicornis colonies on natural reefs. This study examined the survival of 22,634 A. cervicornis colonies raised in nurseries along the Florida reef tract and outplanted to six reef habitats in seven geographical subregions between 2012 and 2018. A Cox proportional hazards regression was used within a Bayesian framework to examine the effects of seven variables: (1) coral‐colony size at outplanting, (2) coral‐colony attachment method, (3) genotypic diversity of outplanted A. cervicornis clusters, (4) reef habitat, (5) geographical subregion, (6) latitude, and (7) the year of monitoring. The best models included coral‐colony size at outplanting, reef habitat, geographical subregion, and the year of monitoring. Survival was highest when colonies were larger than 15 cm (total linear extension), when outplanted to back‐reef and fore‐reef habitats, and when outplanted in Biscayne Bay and Broward–Miami subregions, in the higher latitudes of the Florida reef tract. This study points to several variables that influence the survival of outplanted A. cervicornis colonies and highlights a need to refine restoration strategies to help restore their population along the Florida reef tract.     

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.     

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%.     

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%.     

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.     

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.     

Genotype and attachment technique influence the growth and survival of line nursery corals

The Caribbean staghorn coral, Acropora cervicornis, was once a dominant habitat creating coral, but its populations have declined dramatically in recent decades. Numerous restoration efforts now utilize coral gardening techniques to cultivate this species, growing colonies on fixed structures or from line/suspended nurseries. Line nurseries have become increasingly popular because of their small footprint and ease of use, replacing fixed structures in many nurseries. To evaluate the efficacy of the line technique, this study evaluated growth, condition, and survivorship of A. cervicornis nursery colonies of three distinct genotypes grown via two line nursery techniques (suspended and direct line attachment [vertical]). Direct line attachment of nursery colonies resulted in poor survival (43%) and growth (9.5 ± 1.33 cm/year), whereas suspended culture had 100% survival and increased growth (61.1 ± 4.19 cm/year). Suspended culture had significantly reduced disease prevalence and prevented colony predation. Suspended coral growth was also comparable to a neighboring fixed structure nursery (55.2 ± 7.86 cm/year), and found to be as effective in propagating corals as fixed structures.     

Evaluating Methods for Transplanting Endangered Elkhorn Corals in the Virgin Islands

Restoration of rare corals is desirable and restoration projects are fairly common, but scientific evaluation of this approach is limited. We tested several techniques for transplant and restabilization of Acropora palmata (the elkhorn coral), an ecologically important Caribbean coral whose populations have suffered severe declines. In rough weather, fragments break‐off colonies of branching corals like A. palmata as a normal form of asexual reproduction. We transplanted naturally produced coral fragments from remnant populations to nearby restoration sites. Untouched control fragments at the donor site died faster and grew slower than fragments attached to the reef, so attaching fragments to the reef is beneficial. Transplanted fragments grew and died at a rate similar to fragments left at the donor site (both groups were attached to the reef), so there were no effects of moving fragments or differences in habitat quality between donor and restoration sites. Growth and survival were similar using four methods of attaching fragments to the reef: cable ties, two types of epoxy resin, and hydrostatic cement. Corals sometimes compete with the macroalgae that dominate degraded reefs, and clearing surrounding algae improved the growth of fragments. After 4 years, transplanted fragments grew to 1,450 cm² in area and so were potentially sexually active. Because the methods tested are simple and cheap, they could be used by volunteer recreational divers to restore locally extirpated A. palmata populations or to enhance reefs where natural recovery is slow.     

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.     

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.     

Acclimation in Pocillopora spp. during a coral restoration program in Carrizales Bay,Colima, Mexico

Fragments of the coral Pocillopora spp. were collected from Carrizales Reef to assess two transplantation techniques for coral reef restoration: (1) coral clusters (CC) technique, in which five to seven coral fragments were joined using plastic straps, and (2) simple aggregation (SA) technique, in which fragments were placed evenly on the seabed. Over 270 days, the transplanted fragments were monitored for various indicators of coral health, including skeletal growth, the proportion of colonizing invertebrates, coral fragmentation, the proportion of algal growth, signs of coral disease, and the degree of fusion of coral fragments. We found 95.5% and 89.0% survival of fragments with the CC and SA techniques, respectively. These results indicate that the CC technique leads to greater stability, merger and integration of fragments, and greater aggregation of the fragments with the substrate at transplantation sites. Both transplantation methods are economical and could easily be applied at a broad scale for coral reef restoration.     

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.     

Effects of nursery table slope orientation on coral survival and growth

Transplanting nursery-reared corals is among one of the most common approaches to assist the recovery of degraded reefs. The nursery phase is considered essential for providing a favourable environment for coral fragments to grow into suitable sizes before transplantation to natural reef substrates. Several types of coral nursery designs have been used, but the effect of nursery table slope orientation on survival and growth of coral fragments has not been fully evaluated. Survival and growth of coral fragments from four species (Pectinia paeonia, Podabacia crustacea, Pocillopora acuta, Merulina ampliata) on three inclinations of nursery table top (horizontal (0°), diagonal (45°) and vertical (90°)) were monitored over six months. The effects of slope orientation on survival and growth of fragments were not significant among species except P. acuta, for which survivorship and growth decreased significantly only on vertical nursery tables. The conditions required for coral propagation, such as slope orientation of nursery tables and the initial size of fragments, clearly differ among species due to their inherent attributes and restoration success will greatly benefit from empirical studies derived from a wider range of species.     

Strategies for Gardening Denuded Coral Reef Areas: The Applicability of Using Different Types of Coral Material for Reef Restoration

Recreational and other human activities degrade coral reefs worldwide to a point where efficient restoration techniques are needed. Here we tested several strategies for gardening denuded reefs. The gardening concept consists of in situ or ex situ mariculture of coral recruits, followed by their transplantation into degraded reef sites. In situ nurseries were established in Eilat's (Northern Red Sea) shallow waters, sheltering three types of coral materials taken from the branching species Stylophora pistillata (small colonies, branch fragments, and spat) that were monitored for up to two years. Pruning more than 10% of donor colonies' branches increased mortality, and surviving colonies displayed reduced reproductive activity. Maricultured isolated branches, however, exceeded donor colony life span and reproductive activity and added 0.5–45% skeletal mass per year. Forty‐four percent of the small colonies survived after 1.5‐year mariculture, revealing average yearly growth of 75 ± 32%. Three months ex situ maintenance of coral spat (sexual recruits) prior to the in situ nursery phase increased survivorship. Within the next 1.5 years, they developed into colonies of 3–4 cm diameter. Nursery periods of 2 years, 4–5 years, and more than> 5 years have been estimated for small colonies, spat, and isolated branches, respectively. These and other results, including the possible use of nubbins (minute fragments the size of a single or few polyps), are discussed, revealing benefits and drawbacks for each material. In situ coral mariculture is an improved practice to the common but potentially harmful protocol of direct coral transplantation. It is suggested that reef gardening may be used as a key management tool in conservation and restoration of denuded reef areas. The gardening concept may be applicable for coral reefs worldwide through site‐specific considerations and the use of different local coral species.     

In Situ Coral Nurseries Serve as Genetic Repositories for Coral Reef Restoration after an Extreme Cold‐Water Event

During an unusual cold‐water event in January 2010, reefs along the Florida Reef Tract suffered extensive coral mortality, especially in shallow reef habitats in close proximity to shore and with connections to coastal bays. The threatened staghorn coral, Acropora cervicornis, is the focus of propagation and restoration activities in Florida and one of the species that exhibited high susceptibility to low temperatures. Complete mortality of wild staghorn colonies was documented at 42.9% of donor sites surveyed after the cold event. Remarkably, 72.7% of sites with complete A. cervicornis mortality had fragments surviving within in situ coral nurseries. Thus, coral nurseries served as repositories for genetic material that would have otherwise been completely lost from donor sites. The location of the coral nurseries at deeper habitats and distanced from shallow nearshore habitats that experienced extreme temperature conditions buffered the impacts of the cold‐water event and preserved essential local genotypes for future Acropora restoration activities.     

Employing a highly fragmented,weedy coral species in reef restoration

A major determinant in reef restoration programs is the choice of species employed. In this paper, we concentrate on the potential use of Montipora digitata (Dana, 1846), a highly fragmented and weedy coral species, for reef restoration and for recreation of reef physiognomy in Bolinao, The Philippines, under the ‘gardening concept’. Coral ramets (n = 1960) were reared in a shallow lagoon nursery for 1 year and then, the resulting nursery-grown colonies were transplanted onto denuded reef knolls at two different sites and according to three transplantation designs (grid design with high or low density and patch design). The nursery grown ramets, which had initially exhibited a 99% survivorship, were reduced to 87% by a super typhoon. Low detachment rates, low mortality (<1% both) and low bleaching (<3% over most months), have been indicating good nursery conditions for corals. Monitoring transplanted colonies for over 15 months showed no significant differences between the sites or among the three different transplantation designs. The major events of mortality and detachment were documented during the first 3 months post-transplantation and in the wake of a bleaching event. M. digitata transplants exhibited rapid growth (a 384% increase in ecological volume) and frequent fragmentation. Some fragments remained by their colonies of origin entangled in the attached branches, while other fragments fell onto the surrounding sandy substrate, forming M. digitata ‘beds’ around the knolls. In both, nursery and transplanted corals, creation of complex 3D structures was followed by recruitment of juvenile fishes into aggregations. Above results reveal that employing fast growing, weedy and easily fragmenting branching species, which are also considered as ‘modifier species’, in reef restoration may result in a fast regeneration of reef physiognomy. Instead of ‘copying’ natural processes, reef managers should therefore concentrate on recovering the reef's ability for self-maintenance.     

Poor Performance of Corals Transplanted onto Substrates of Short Durability

Worldwide, coral reefs are degrading due to increasing anthropogenic pressures. Yet, management of reefs still falls short of effectively addressing these threats, and active restoration methods are increasingly being called for. Coral transplantation is frequently advocated as a possible means of coral reef rehabilitation. Fragments produced in coral nurseries or farms have been proposed as a potential source for transplantation, and culture media (inexpensive but non‐durable materials such as wood or bamboo) may serve as transplantation substrate if placed directly in the reef. However, the performance of coral transplants attached to such substrates has not been examined yet. Here, the long‐term survival of transplants attached to bamboo substrates is reported. A total of 6,164 fragments of 4 coral species (Acroporids and Pocilloporids) were monitored for up to 20 months at three sites in North Sulawesi/Indonesia. Bamboo failed as a suitable inexpensive substrate in at least two of the three sites examined. Mortality of transplants 2 years after transplantation was high in three of the four species (67–95%) and was partially linked to substrate disintegration. The results show that, in places were currents or waves threaten to dislocate transplants, a higher effort needs to be directed at a strong and durable attachment of transplanted corals.     

Simple ecological trade-offs give rise to emergent cross-ecosystem distributions of a coral reef fish

Ecosystems are intricately linked by the flow of organisms across their boundaries, and such connectivity can be essential to the structure and function of the linked ecosystems. For example, many coral reef fish populations are maintained by the movement of individuals from spatially segregated juvenile habitats (i.e., nurseries, such as mangroves and seagrass beds) to areas preferred by adults. It is presumed that nursery habitats provide for faster growth (higher food availability) and/or low predation risk for juveniles, but empirical data supporting this hypothesis is surprisingly lacking for coral reef fishes. Here, we investigate potential mechanisms (growth, predation risk, and reproductive investment) that give rise to the distribution patterns of a common Caribbean reef fish species, Haemulon flavolineatum (French grunt). Adults were primarily found on coral reefs, whereas juvenile fish only occurred in non-reef habitats. Contrary to our initial expectations, analysis of length-at-age revealed that growth rates were highest on coral reefs and not within nursery habitats. Survival rates in tethering trials were 0% for small juvenile fish transplanted to coral reefs and 24-47% in the nurseries. As fish grew, survival rates on coral reefs approached those in non-reef habitats (56 vs. 77-100%, respectively). As such, predation seems to be the primary factor driving across-ecosystem distributions of this fish, and thus the primary reason why mangrove and seagrass habitats function as nursery habitat. Identifying the mechanisms that lead to such distributions is critical to develop appropriate conservation initiatives, identify essential fish habitat, and predict impacts associated with environmental change.     

Effects of marine reserves versus nursery habitat availability on structure of reef fish communities

No-take marine fishery reserves sustain commercial stocks by acting as buffers against overexploitation and enhancing fishery catches in adjacent areas through spillover. Likewise, nursery habitats such as mangroves enhance populations of some species in adjacent habitats. However, there is lack of understanding of the magnitude of stock enhancement and the effects on community structure when both protection from fishing and access to nurseries concurrently act as drivers of fish population dynamics. In this study we test the separate as well as interactive effects of marine reserves and nursery habitat proximity on structure and abundance of coral reef fish communities. Reserves had no effect on fish community composition, while proximity to nursery habitat only had a significant effect on community structure of species that use mangroves or seagrass beds as nurseries. In terms of reef fish biomass, proximity to nursery habitat by far outweighed (biomass 249% higher than that in areas with no nursery access) the effects of protection from fishing in reserves (biomass 21% lower than non-reserve areas) for small nursery fish (≤ 25 cm total length). For large-bodied individuals of nursery species (>25 cm total length), an additive effect was present for these two factors, although fish benefited more from fishing protection (203% higher biomass) than from proximity to nurseries (139% higher). The magnitude of elevated biomass for small fish on coral reefs due to proximity to nurseries was such that nursery habitats seem able to overrule the usually positive effects on fish biomass by reef reserves. As a result, conservation of nursery habitats gains importance and more consideration should be given to the ecological processes that occur along nursery-reef boundaries that connect neighboring ecosystems.