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%.     

Location‐Specific Metrics for Rapidly Estimating the Abundance and Condition of the Threatened Coral Acropora cervicornis

We developed a method for quantifying the abundance of the threatened staghorn coral (Acropora cervicornis) and evaluated the accuracy of commonly used methods to assess colony condition. For small‐ to medium‐sized colonies, we show that colony ellipsoid volume estimated from simple colony dimensions serves as a reliable and efficient proxy for the more time‐consuming, conventional measure of colony total linear extension, and that this predictive relationship varies significantly among extant populations in the Caribbean. We also determined that visual estimates of colony partial mortality closely approximate to true values for colonies with <25% mortality, with in situ estimates outperforming estimates from digital images. These results provide coral reef managers and restoration practitioners with guidance for assessing partial mortality and location‐specific regression models to estimate “amount” of staghorn coral in both extant and restored staghorn populations in Belize, the United States Virgin Islands, and the Dry Tortugas National Park, Florida, U.S.A. As staghorn coral monitoring and restoration efforts continue to expand in the Caribbean, these methods for quickly determining staghorn abundance and condition will directly aid resource managers tasked with monitoring wild populations and tracking restoration success over time.     

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.     

Ecological impacts of coral gardening outplanting in the Maldives

As coral reefs continue to degrade at an alarming rate, coral restoration efforts are increasing worldwide in an attempt to keep up with the global challenge of preserving these iconic ecosystems and the many services they provide. Coral gardening, the farming and outplanting of coral fragments, is a commonly applied practice; however, regional validation is required before upscaling can be considered. This study follows up from the successful farming of fragments in mid-water rope nurseries, by reporting on the successive outplanting of these corals. Specifically, 60 Pocillopora verrucosa colonies were outplanted to a degraded reef at different depths (1–12 m), applying three arrangement patterns (equal, clustered, random). After 1 year, 72% were considered successfully outplanted (alive and still attached), with detachment being the main challenge at wave-impacted shallow depths, while loose coral rubble caused more partial mortality at depth. Outplanting stress was observed at 1–6 m depth, but had no impact on survival or growth. Drupella sp. predation was most common at 3 m and 79% of colonies hosted mutualistic fauna after 1 year. Outplanting significantly benefitted the reef environment with a higher fish abundance and diversity along with a higher increase in natural coral cover (H = 2.7; 6.2% increase) in comparison with the control sites. These are promising results, considering that the restoration site has shown little natural recovery in the last few years (coral cover <4%). We hope that our findings provide useful initial insights and help to guide effective restoration practices in the Maldives.     

Feasibility of early outplanting of sexually propagated Acropora verweyi for coral reef restoration demonstrated in the Philippines

Over the last 20 years, coral sexual propagation techniques for reef restoration have been steadily developed and improved. However, these techniques involve considerable time and costs to grow coral propagules. There is a need to examine the optimal size of juvenile corals for outplantation. Here, we outplanted sexually propagated small (3–5 mm diameter) and large (10–15 mm diameter) Acropora verweyi corals at 4 months after fertilization at two sites in northwestern Philippines, and compared their survival and radial growth rate after a year. A. verweyi coral juveniles (n = 240) exhibited an overall mean survival of 29.5% and growth rate of 11.12 ± 6.2 mm/year (mean ± SD). Large colonies had a significantly higher growth rate than smaller colonies. Although survivorship of large juveniles was significantly better than that of the smaller ones at one site, it did not differ significantly at the other. Each 4‐month‐old coral cost US$1.52 to produce, while the cost of each of the outplanted juveniles (n = 240) was about US$2.67, whereas the cost of each survivor about a year after outplantation was US$11.47. Results suggest that A. verweyi reared in ex situ nurseries for only 4 months can survive reasonably well when outplanted onto coral reefs.     

Host population genetic structure and zooxanthellae diversity of two reef-building coral species along the Florida Reef Tract and wider Caribbean

In preparation for a large-scale coral restoration project, we surveyed host population genetic structure and symbiont diversity of two reef-building corals in four reef zones along the Florida reef tract (FRT). There was no evidence for coral population subdivision along the FRT in Acropora cervicornis or Montastraea faveolata based on microsatellite markers. However, in A. cervicornis, significant genetic differentiation was apparent when extending the analysis to broader scales (Caribbean). Clade diversity of the zooxanthellae differed along the FRT. A. cervicornis harbored mostly clade A with clade D zooxanthellae being prominent in colonies growing inshore and in the mid-channel zones that experience greater temperature fluctuations and receive significant nutrient and sediment input. M. faveolata harbored a more diverse array of symbionts, and variation in symbiont diversity among four habitat zones was more subtle but still significant. Implications of these results are discussed for ongoing restoration and conservation work.     

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.     

Outplanting of branching Acropora enhances recolonization of a fish species and protects massive corals from predation

Damselfish of the genus Stegastes inhabit territories and cultivate algal gardens on branching corals of the genus Acropora, aggressively protecting their territories from other fish and preventing predation upon corals within the territory. This behaviour has important ecological impacts and could also be useful in reducing predation on outplanted corals during reef restoration efforts. However, the degree of protection from predators may depend on the ability of Stegastes spp. to recolonise outplanted or newly established coral colonies. Protection of bleaching-resilient massive corals within territories may be of particular importance due to the role of these corals in maintaining coral cover following bleaching events. This study examined whether the presence of Stegastes spp. reduces predation on the massive bleaching-resilient coral Porites lutea in the Mauritian lagoon, and whether Stegastes spp. readily colonise outplanted branching coral fragments and provide adjacent massive corals with indirect protection from predation. Predation levels on wild-occurring and outplanted P. lutea within and outside Stegastes spp. territories were measured. In addition, Acropora muricata branches were outplanted adjacent to wild P. lutea colonies outside Stegastes spp. territories, and recolonisation of these outplants by Stegastes spp. and the impacts of recolonisation on predation were monitored. Both wild and outplanted P. lutea colonies within Stegastes spp. territories sustained less predation damage compared to colonies outside territories. Stegastes spp. recolonized outplanted A. muricata colonies within six months of outplanting, and in doing so returned predation protection to adjacent P. lutea colonies. The ability of Stegastes spp. to colonise outplanted corals and provide indirect protection to adjacent massive bleaching-resilient corals may inform coral outplanting efforts in systems where Stegastes spp. are common. Encouraging Stegastes spp. recolonisation may help to reduce predation damage to corals within territories and potentially improve the success of rehabilitation efforts.

     

Occupation Dynamics and Impacts of Damselfish Territoriality on Recovering Populations of the Threatened Staghorn Coral,Acropora cervicornis

Large-scale coral reef restoration is needed to help recover structure and function of degraded coral reef ecosystems and mitigate continued coral declines. In situ coral propagation and reef restoration efforts have scaled up significantly in past decades, particularly for the threatened Caribbean staghorn coral, Acropora cervicornis, but little is known about the role that native competitors and predators, such as farming damselfishes, have on the success of restoration. Steep declines in A. cervicornis abundance may have concentrated the negative impacts of damselfish algal farming on a much lower number of coral prey/colonies, thus creating a significant threat to the persistence and recovery of depleted coral populations. This is the first study to document the prevalence of resident damselfishes and negative effects of algal lawns on A. cervicornis along the Florida Reef Tract (FRT). Impacts of damselfish lawns on A. cervicornis colonies were more prevalent (21.6% of colonies) than those of other sources of mortality (i.e., disease (1.6%), algal/sponge overgrowth (5.6%), and corallivore predation (7.9%)), and damselfish activities caused the highest levels of tissue mortality (34.6%) among all coral stressors evaluated. The probability of damselfish occupation increased as coral colony size and complexity increased and coral growth rates were significantly lower in colonies with damselfish lawns (15.4 vs. 29.6 cm per year). Reduced growth and mortality of existing A. cervicornis populations may have a significant effect on population dynamics by potentially reducing important genetic diversity and the reproductive potential of depleted populations. On a positive note, however, the presence of resident damselfishes decreased predation by other corallivores, such as Coralliophila and Hermodice, and may offset some negative impacts caused by algal farming. While most negative impacts of damselfishes identified in this study affected large individual colonies and <50% of the A. cervicornis population along the FRT, the remaining wild staghorn population, along with the rapidly increasing restored populations, continue to fulfill important functional roles on coral reefs by providing essential habitat and refuge to other reef organisms. Although the effects of damselfish predation are, and will continue to be, pervasive, successful restoration efforts and strategic coral transplantation designs may help overcome damselfish damage by rapidly increasing A. cervicornis cover and abundance while also providing important information to educate future conservation and management decisions.     

Outplanting optimized: developing a more efficient coral attachment technique using Portland cement

Coral reefs are among the most valuable and vulnerable ecosystems on Earth. Their decline has spurred global interest in efforts to augment native coral populations through coral gardening. As these efforts expand, practitioners are constantly looking for new techniques to reduce costs and increase their restoration footprint. However, commonly employed coral attachment methods limit the numbers of corals that can be outplanted per day, representing a substantial bottleneck in the coral restoration process. Cement has potential as a more cost‐ and time‐efficient coral attachment technique, but research is needed to understand its effects on coral survivorship and develop best practices for its use. Here, we use lab and field tests in a three‐stage elimination format to determine the most effective cement mixture for outplanting Acropora cervicornis. We then compare this new method to two commonly used coral attachment techniques: the nail and cable tie method and two‐part epoxy putty. Our tests identified the optimal cement mix to be a combination of 10 parts type I/II Portland cement to one part silica fume. This mix yielded equivalent survivorship to the other two methods, is quick and easy to use making it ideal for citizen scientists, and has roughly one‐tenth of the material cost of other methods. These results support the wider use of cement for coral outplanting in order to minimize costs, maximize efficiency, and increase the effectiveness of coral restoration efforts around the world.     

Optimizing return‐on‐effort for coral nursery and outplanting practices to aid restoration of the Great Barrier Reef

Coral nursery and outplanting practices have grown in popularity worldwide for targeted restoration of degraded “high value” reef sites, and recovery of threatened taxa. Success of these practices is commonly gauged from coral propagule growth and survival, which fundamentally determines the return‐on‐effort (RRE) critical to the cost‐effectiveness and viability of restoration programs. In many cases, RRE has been optimized from past successes and failures, which therefore presents a major challenge for locations such as the Great Barrier Reef (GBR) where no local history of restoration exists to guide best practice. In establishing the first multi‐taxa coral nursery on the GBR (Opal Reef, February 2018), we constructed a novel scoring criterion from concurrent measurements of growth and survivorship to guide our relative RRE, including nursery propagule numbers (stock density). We initially retrieved RRE scores from a database of global restoration efforts to date (n = 246; 52 studies) to evaluate whether and how success commonly varied among coral taxa. We then retrieved RRE scores for Opal Reef using initial growth and survivorship data for six key coral taxa, to demonstrate that RRE scores were high for all taxa predominantly via high survivorship over winter. Repeated RRE scoring in summer is therefore needed to capture the full dynamic range of success where seasonal factors regulating growth versus survivorship differ. We discuss how RRE scoring can be easily adopted across restoration practices globally to standardize and benchmark success, but also as a tool to aid decision‐making in optimizing future propagation (and outplanting) efforts.     

How Quickly do Fragments of Coral “Self‐Attach” after Transplantation?

Transplantation of coral fragments is seen as a potential method to rapidly restore coral cover to areas of degraded reef; however, considerable research is still needed to assess the effectiveness of coral transplantation as a viable reef restoration tool. Initially, during restoration efforts, coral transplants are attached artificially. Self‐attachment (i.e., growth of coral tissue onto the substrate) provides a more secure and lasting bond, thus knowledge about self‐attachment times for corals is of importance to reef restoration. While it is known that coral fragments may generate new tissue and bond to substrata within a few weeks of transplantation, surprisingly little is known about the speed of self‐attachment for most species. Two independent experiments were carried out to examine the self‐attachment times of 12 scleractinian and one non‐scleractinian coral species to a natural calcium carbonate substrate. The first experiment examined times to self‐attachment in 11 species of differing morphologies from seven families over approximately 7 months, whereas the second experiment examined three fast‐attaching Acropora species over approximately 1 month. In the first experiment, the branching species Acropora muricata had a significantly faster self‐attachment time compared to all other species, while Echinopora lamellosa had the slowest self‐attachment time. For the second experiment, A. muricata was significantly slower to self‐attach than Acropora hyacinthus (tabular) and Acropora digitifera (corymbose‐digitate). The results suggest that a combination of factors including growth rates, growth form and life history may determine how quickly fragments of coral species self‐attach after fragmentation and transplantation.     

Density‐dependent effects on initial growth of a branching coral under restoration

Coral reef restoration aims to help threatened coral ecosystems recover from recent severe declines. Here we address whether coral fragments should be out‐planted individually or in larger aggregations. Theory suggests alternative possible outcomes: whereas out‐plants within aggregations might suffer from heightened negative interactions with neighbors (e.g. competition for space), they may alternatively benefit from positive interactions with neighbors (e.g. buffering wave disturbances). On a degraded reef in the Caribbean (St. Croix, USVI), using out‐plants of the critically endangered staghorn coral Acropora cervicornis, we experimentally tested how aggregation density (1–20 out‐planted coral fragments spaced at approximately 5 cm) influenced initial coral growth (over 3 months). Coral growth declined as a function of aggregation size, and out‐plants within larger aggregations had fewer and shorter secondary branches on average, indicative of horizontal competition for space. Our results therefore suggest that wide spacing of individuals will maximize the initial growth of out‐planted branching corals.     

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.     

Genetic relatedness does not retain spatial pattern across multiple spatial scales: dispersal and colonization in the coral,Pocillopora damicornis

Patterns of isolation by distance are uncommon in coral populations. Here, we depart from historical trends of large‐scale, geographical genetic analyses by scaling down to a single patch reef in Kāne‘ohe Bay, Hawai‘i, USA, and map and genotype all colonies of the coral, Pocillopora damicornis. Six polymorphic microsatellite loci were used to assess population genetic and clonal structure and to calculate individual colony pairwise relatedness values. Our results point to an inbred, highly clonal reef (between 53 and 116 clonal lineages of 2352 genotyped colonies) with a much skewed genet frequency distribution (over 70% of the reef was composed of just seven genotypes). Spatial autocorrelation analyses revealed that corals found close together on the reef were more genetically related than corals further apart. Spatial genetic structure disappears, however, as spatial scale increases and then becomes negative at the largest distances. Stratified, random sampling of three neighbouring reefs confirms that reefs are demographically open and inter‐reef genetic structuring was not detected. Attributing process to pattern in corals is complicated by their mixed reproductive strategies. Separate autocorrelation analyses, however, show that the spatial distribution of both clones and nonclones contributes to spatial genetic structure. Overall, we demonstrate genetic structure on an intrareef scale and genetic panmixia on an inter‐reef scale indicating that, for P. damicornis, the effect of small‐ and large‐scale dispersal processes on genetic diversity are not the same. By starting from an interindividual, intrareef level before scaling up to an inter‐reef level, this study demonstrates that isolation‐by‐distance patterns for the coral P. damicornis are limited to small scales and highlights the importance of investigating genetic patterns and ecological processes at multiple scales.     

Potential feedback between coral presence and farmerfish collective behavior promotes coral recovery

Stable between‐group differences in collective behavior have been documented in a variety of social taxa. Here we evaluate the effects of such variation, often termed collective or colony‐level personality, on coral recovery in a tropical marine farmerfish system. Groups of the farmerfish Stegastes nigricans cultivate and defend gardens of palatable algae on coral reefs in the Indo‐Pacific. These gardens can promote the recruitment, growth, and survival of corals by providing a refuge from coral predation. Here we experimentally evaluate whether the collective response of farmerfish colonies is correlated across intruder feeding guilds – herbivores, corallivores and egg‐eating predators. Further, we evaluate if overall colony responsiveness or situation‐specific responsiveness (i.e. towards herbivores, corallivores, or egg‐eaters in particular) best predicts the growth of outplanted corals. Finally, we experimentally manipulated communities within S. nigricans gardens, adding either macroalgae or large colonies of coral, to assess if farmerfish behavior changes in response to the communities they occupy. Between‐group differences in collective responsiveness were repeatable across intruder guilds. Despite this consistency, responsiveness towards corallivores (porcupinefish and ornate butterflyfish) was a better predictor of outplanted coral growth than responsiveness towards herbivores or egg‐eaters. Adding large corals to farmerfish gardens increased farmerfish attacks towards intruders, pointing to possible positive feedback loops between their aggression towards intruders and the presence of corals whose growth they facilitate. These data provide evidence that among‐group behavioral variation could strongly influence the ecological properties of whole communities.     

Millennial-scale dynamics of staghorn coral in Discovery Bay, Jamaica

Populations of the staghorn coral, Acropora cervicornis, collapsed throughout the Caribbean region from the late 1970s through the 1990s. We tested the hypothesis that this recent, multidecadal interruption in coral growth was a novel event in the late Holocene. Eight cores, extracted from a lagoonal reef in Discovery Bay, Jamaica dated to 440–1260 CalBP and consisted almost entirely of A. cervicornis rubble. The A. cervicornis in the cores showed significantly less internal bioerosion than A. cervicornis from modern death assemblages in Discovery Bay, indicating generally shorter post‐mortem exposure at the sediment–water interface in the past. A. cervicornis grew continuously and was buried rapidly during the millennium preceding the 1980s, with the exception of a possible hiatus in growth and burial at some point 300–600 years ago. In the 1980s, a combination of perturbations, which included overfishing and (possibly) other forms of human interference, caused an unprecedented disruption in the growth and burial of staghorn coral populations in Discovery Bay.     

Near‐term impacts of coral restoration on target species,coral reef community structure,and ecological processes

The global decline of corals has created an urgent need for effective, science‐based methods to augment coral populations and restore important ecosystem functions. To meet this challenge, the field of coral restoration has rapidly evolved over the past decade. However, despite widespread efforts to outplant corals and monitor survivorship, there is a shortage of information on the effects of coral restoration on reef communities or important ecosystem functions. To fill this knowledge gap, we examined the effects of restoration on three major criteria: diversity, community structure, and ecological processes. We conducted surveys of four restored sites in the Florida Keys ranging in restoration effort (500–2,300 corals outplanted) paired with surveys of nearby, unmanipulated control sites. Coral restoration successfully enhanced coral populations, increasing coral cover 4‐fold, but manifested in limited differences in coral and fish communities. Some restored sites had higher abundance of herbivorous fish, rates of herbivory, or more juvenile‐sized corals, but these effects were limited to individual reefs. Damselfish were consistently more abundant at restored compared to control sites. Despite augmenting target coral populations, 3 years of coral restoration has not facilitated many of the positive feedbacks that help reinforce coral success. In a time of increasingly frequent disturbances, it is urgent we hasten the speed at which reefs recover important ecological processes, such as herbivory and nutrient cycling, that make reefs more resistant and resilient if we are to achieve long‐term restoration success.     

Coralclip®: a low‐cost solution for rapid and targeted out‐planting of coral at scale

Re‐attaching or out‐planting coral as fragments, colonies, and on larval settlement devices to substrates is a major bottleneck limiting scalabilty and viability of reef restoration practices. Many attachment approaches are in use, but none that are low‐cost, opportunistic, rapid but effective, for integration into existing tour operations on the Great Barrier Reef (GBR) where staff and boat time is a major cost and chemical fixatives cannot be easily used. We describe a novel attachment device—Coralclip®—developed to meet this need and so aid maintenance and restoration of GBR tourism sites. Coralclip® is a stainless steel springclip attached by a nail integrated through the spring coil, and can be deployed with a coral fragment in as fast as 15 seconds. Initial laboratory tests demonstrated that Coralclip® secured coral fragments or larval settlement tiles under dynamic flow regimes characteristic of exposed reefs. Coral out‐planting from fragments of opportunity and from nurseries (n = 4,580; 0.3–1.9 coral/minute; US$0.6–3.0/coral deployed) or larval settlement tiles (n = 400; 2.5 tiles/minute; US$0.5 tile deployed^?1) when deployed by divers from routine boat operations at Opal Reef confirmed highly effective attachment, with ≤15% failure of clips found after 3–7 months. We discuss how Coralclip® is a cost‐effective means to support reef maintenance and restoration practices.