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%.     

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.     

Polyp oriented modelling of coral growth

The morphogenesis of colonial stony corals is the result of the collective behaviour of many coral polyps depositing coral skeleton on top of the old skeleton on which they live. Yet, models of coral growth often consider the polyps as a single continuous surface. In the present work, the polyps are modelled individually. Each polyp takes up resources, deposits skeleton, buds off new polyps and dies. In this polyp oriented model, spontaneous branching occurs. We argue that branching is caused by a so called “polyp fanning effect” by which polyps on a convex surface have a competitive advantage relative to polyps on a flat or concave surface. The fanning effect generates a more potent branching mechanism than the Laplacian growth mechanism that we have studied previously (J. Theor. Biol. 224 (2003) 153). We discuss the application of the polyp oriented model to the study of environmentally driven morphological plasticity in stony corals. In a few examples we show how the properties of the individual polyps influence the whole colony morphology. In our model, the spacing of polyps influences the thickness of coral branches and the overall compactness of the colony. Density variations in the coral skeleton may also be important for the whole colony morphology, which we address by studying two variants of the model. Finally, we discuss the importance of small scale resource translocation in the coral colony and its effects on the morphology of the colony.     

Ontogenetic changes in the capacity of the coral Pocillopora damicornis to originate branches

Most colonial corals vary intraspecifically in growth forms, and the diversity in branching morphology is especially striking. While the effects of environmental factors on growth forms have been studied, the genetic control of coral branching patterns has received little attention. The discovery of ontogenetic changes in the capacity to originate branching would set the stage for studies of how branch formation is genetically controlled. During experiments investigating contact reactions in the coral Pocillopora damicornis, we observed that young colonies derived from settled planulae and colonies regenerated from adult branch tips assumed different growth forms. Young colonies formed at least one branch from the central region of the colony, while colonies regenerated from adult branch tips (3-5 mm long) did not form branches during the 9-month observation period. This pattern was invariable, regardless of the types and outcomes of the contact experiments or the orientation of the branch tips. However, some fragments taken from 1- or 2-year-old colonies formed branches. This suggests that the rate of branch formation in P. damicornis colonies decreases with age. These findings will facilitate investigations of the mechanism of coral branch formation at the molecular level.     

Transplantation and cultivation of fragments of coral colonies of various scleractinian species on a reef in Vietnam

Six coral species of the genus Acropora and two species of the genus Porites were studied during experiments on cultivation of reef-building scleractinian corals. The research has established species-specific factors and others affecting regeneration of fragments and growth of new colonies in these coral species. The accretion of donor fragments and new branches averaged from 40 to 160 mm per year, depending on the coral species, colony size, and season of transplantation. An average monthly accretion of medium and larger transplants and growth of new branches were 1.2–1.3 times higher at spring cultivation than at autumn transplanting. When transplanted, coral fragments of medium and larger sizes survived well and showed higher growth rates in all species studied. These transplants developed the highest number of new branches, and their buds and formed the largest colonies. Prolongation of the cultivation time from 1 to 1.5 years caused a 1.2–1.4 fold accretion of transplants.     

Effects of frequent fish predation on corals in Hawaii

The abundance of lesions from fish bites on corals was quantified at nine shallow reefs in the main Hawaiian Islands. There were on average 117 bite scars m⁻² on Pocillopora meandrina tissue from the barred filefish Cantherhines dumerilii, 69 bites m⁻² on Porites compressa tissue, and 4 bites m⁻² on Porites lobata tissue from the spotted puffer Arothron meleagris. Across sites, the frequency of A. meleagris bites on P. compressa per unit area of living coral cover declined exponentially with increasing coral cover. P. compressa nubbins in two size classes (1–2 cm and 4–5 cm) were transplanted onto six study reefs. Nubbins in the small size class were entirely removed by bites from A. meleagris, while nubbins ≥4 cm were only partially consumed, leaving them able to recover. At sites with abundant P. compressa, predation had little effect on transplanted nubbins; at sites where P. compressa comprised less than 5% of living cover, all nubbins were preyed upon. A. meleagris bite lesions on P. compressa were monitored through time and fully recovered in 42 ± 4 days. A model of the risk of over-predation (a second predation event before the first is healed) decreased exponentially with increasing coral cover and increased linearly with increasing lesion healing time. The increased risk of over-predation at low coral cover could indicate an Allee effect limiting the recovery of coral populations if coral cover is substantially reduced by natural or anthropogenic disturbances.     

Optimizing industrial‐scale coral reef restoration: comparing harvesting wild coral spawn slicks and transplanting gravid adult colonies

Accelerating coral reef restoration is a global challenge that has been attempted around the world. Previous attempts show varying levels of success at localized scales, but comparisons of cost and benefits to evaluate large‐scale reef restoration approaches are lacking. Here, we compare two large‐scale restoration approaches: the harvesting, development, and release of wild coral spawn slicks onto a target reef, with the transplantation of gravid coral colonies to provide a seed population and local source of larvae. Comparisons incorporate the best available information on demographic rates to estimate population growth, beginning at embryo production to colony maturity 4 years following deployment. Cost‐effectiveness is considered in a coarse manner. The harvesting, development, and controlled release of coral spawn slicks is anticipated to achieve large‐scale restoration of coral communities with low‐impact technology at low cost per colony. Harvesting wild spawn slicks has the potential to (1) transport billions of larvae up to thousands of kilometers that (2) are relevant to coral restoration efforts at vast geographical scales while (3) benefitting from the use of technology with extremely low impact on wild populations and (4) retaining natural genetic and species diversity needed to enhance the resilience of restored communities. Transplanting colonies is most useful from reefs designated to be impacted by infrastructural development by providing an opportunity for transfer to high value zones, from dedicated nurseries, and for brooding species. Our contribution provides insights into critical elements of both concepts, and we highlight information gaps in parameter uncertainties.     

Propagation of the threatened staghorn coral Acropora cervicornis: methods to minimize the impacts of fragment collection and maximize production

Coral reef restoration methods such as coral gardening are becoming increasingly considered as viable options to mitigate reef degradation and enhance recovery of depleted coral populations. In this study, we describe several aspects of the coral gardening approach that demonstrate this methodology is an effective way of propagating the threatened Caribbean staghorn coral Acropora cervicornis: (1) the growth of colonies within the nursery exceeded the growth rates of wild staghorn colonies in the same region; (2) the collection of branch tips did not result in any further mortality to the donor colonies beyond the coral removed for transplantation; (3) decreases in linear extension of the donor branches were only temporary and donor branches grew faster than control branches after an initial recovery period of approximately 3–6 weeks; (4) fragmentation did not affect the growth rates of non-donor branches within the same colony; (5) small branch tips experienced initial mortality due to handling and transportation but surviving tips grew well over time; and (6) when the growth of the branch tips is added to the regrowth of the fragmented donor branches, the new coral produced was 1.4–1.8 times more than new growth in undisturbed colonies. Based on these results, the collection of small (2.5–3.5 cm) branch tips was an effective propagation method for this branching coral species resulting in increased biomass accumulation and limited damage to parental stocks.     

Combined ocean acidification and low temperature stressors cause coral mortality

Oceans are predicted to become more acidic and experience more temperature variability—both hot and cold—as climate changes. Ocean acidification negatively impacts reef-building corals, especially when interacting with other stressors such as elevated temperature. However, the effects of combined acidification and low temperature stress have yet to be assessed. Here, we exposed nubbins of the scleractinian coral Montipora digitata to ecologically relevant acidic, cold, or combined stress for 2 weeks. Coral nubbins exhibited 100% survival in isolated acidic and cold treatments, but ~30% mortality under combined conditions. These results provide further evidence that coupled stressors have an interactive effect on coral physiology, and reveal that corals in colder environments are also susceptible to the deleterious impacts of coupled ocean acidification and thermal stress.     

Detachment of Porites cylindrica nubbins by herbivorous fishes

A form of active restoration for coral assemblages involves culturing coral nubbins at nursery sites before transplantation to recipient reefs. Incidental grazing and/or directed predation by local fish assemblages are major sources of dislodgement and mortality for coral nubbins in nurseries. However, the rate of coral nubbin detachment, how this varies across fish taxa, and whether nubbin size affects rates of detachment warrant further investigation. We used field and aquaria experiments to examine the effect of incidental grazing and predation on the detachment of Porites cylindrica nubbins of different sizes (0.5, 1, 2, 3, 4, and 5 cm height). Short‐term (6 hours) exposure of nubbins to local fish assemblages at Lucero Reef, northwestern Philippines, caused higher detachment (1.93% ± 0.53 SE) compared to caged controls (0.16% ± 0.16 SE), with no detectable effect of nubbin size. To identify the impact of individual fish species, nubbins were exposed to one of four locally abundant herbivorous and corallivorous fish species in aquaria for 8 hours. Nubbin detachment was greater when exposed to Chlorurus spilurus (1.20–36.2%) and Siganus fuscescens (0.00–15.0%) than Chaetodon lunulatus (0.00–4.00%) and Chaetodon kleinii (0.00–1.20%), with the smallest nubbins (0.5 cm) being the most vulnerable. Our results suggest that incidental grazing by herbivorous fishes, especially parrotfishes, may potentially be an important source of detachment and likely mortality of nubbins. Optimizing coral nursery protocols should consider potential trade‐offs between excluding grazing fishes and the accumulation of algal material on caging structures to minimize nubbin mortality and improve coral restoration success.     

Fine structure analysis of black band disease (BBD) infected coral and coral exposed to the BBD toxins microcystin and sulfide

Black band disease (BBD) of corals is a complex pathogenic polymicrobial mat community that lyses coral tissue as it migrates over an infected colony. Two known toxins are produced by BBD microorganisms - sulfide, produced by sulfate-reducing bacteria, and microcystin, produced by cyanobacteria. Experiments were carried out to determine the effects of exposing healthy coral fragments to variable concentrations of purified microcystin, sulfide at a concentration known to exist in BBD, and a combination of the two. Healthy fragments of the coral Montastraea annularis were placed into experimental chambers with known toxin/s for 18-22.5 h. Fine structural analysis using scanning electron microscopy (SEM) showed that toxin exposure resulted in thinning or removal of the coral epidermal layer coupled with degradation of the gastrodermis. These effects were exacerbated when both toxins were used in combination. Exposure to sulfide and the highest concentration of microcystin caused zooxanthellae to dissociate from the coral tissue and to form clusters on the coral surface. Examination of coral fragments infected with BBD was carried out for comparison. It was determined that the effects of exposure to sulfide and microcystin on coral fine structure were consistent, both quantitatively and qualitatively, with the effects of artificially induced and naturally occurring BBD on M. annularis.     

Culture and differentiation of osteoblasts on coral scaffold from human bone marrow mesenchymal stem cells

In this paper we describe an approach that aims to provide fundamental information towards a scientific, biomechanical basis for the use of natural coral scaffolds to initiate mesenchymal stem cells into osteogenic differentiation for transplant purposes. Biomaterial, such as corals, is an osteoconductive material that can be used to home human derived stem cells for clinical regenerative purposes. In bone transplantation, the use of biomaterials may be a solution to bypass two main critical obstacles, the shortage of donor sites for autografts and the risk of rejection with allograft procedures. Bone regeneration is often needed for multiple clinical purposes for instance, in aesthetic reconstruction and regenerative procedures. Coral graft Porites lutea has been used by our team for a decade in clinical applications on over a thousand patients with different bone pathologies including spinal stenosis and mandibular reconstruction. It is well accepted that human bone marrow (hBM) is an exceptional source of mesenchymal stem cells (MSCs), which may differentiate into different cell phenotypes such as osteoblasts, chondrocytes, adipocytes, myocytes, cardiomyocytes and neurons. Isolated MSCs from human bone marrow were induced into osteoblasts using an osteogenic medium enriched with two specific growth factors, FGF9 and vitamin D2. Part of the cultured MSCs were directly transferred and seeded onto coral scaffolds (Porites Lutea) and induced to differentiate into osteoblasts and part were cultured in flasks for osteocell culture. The data support the concept that hBM is a reliable source of MSCs which may be easily differentiated into osteoblasts and seeded into coral as an optimal device for clinical application. Within this project we have also discussed the biological nature of MSCs, their potential application for clinical transplantation and the prospect of their use in gene therapy.     

Natural inducers for coral larval metamorphosis

 Coral gametes from Acropora millepora (Ehrenberg, 1834) and from multi-species spawning slicks provided larvae for use in metamorphosis assays with a selection of naturally occurring inducer chemicals. Four species of crustose coralline algae, one non-coralline crustose alga and two branching coralline algae induced larval metamorphosis. However, one additional species of branching coralline algae did not produce a larval response. Metamorphosis was also observed when larvae were exposed to skeleton from the massive coral Goniastrea retiformis (Lamarck, 1816) and to calcified reef rubble, demonstrating metamorphosis is possible in the absence of encrusting algae. Chemical extracts from these algae and the coral skeleton, obtained using either decalcification or simple methanol extraction procedures, also contained active inducers. These results extend the number of crustose algal species known to induce coral metamorphosis, suggest that some inducers may not necessarily be strongly associated with the calcified algal cell walls, and indicate that inducer sources in reef habitats may be more diverse than previously reported. Accepted: 21 May 1999     

Differential thermal bleaching susceptibilities amongst coral taxa: re-posing the role of the host

It is well established that different coral species have different susceptibilities to thermal stress, yet it is less clear which biological or physical mechanisms allow some corals to resist thermal stress, whereas other corals bleach and die. Although the type of symbiont is clearly of fundamental importance, many aspects of coral bleaching cannot be explained solely by differences in symbionts amongst coral species. Here, I use the CO₂ (sink) limitation model of coral bleaching to repose various host traits believed to influence thermal tolerance (e.g. metabolic rates, colony tissue thickness, skeletal growth form, mucus production rates, tissue concentration of fluorescent pigments and heterotrophic feedings capacity) in terms of an integrated strategy to reduce the likelihood of CO₂ limitation around its intracellular photosymbionts. Contrasting observational data for the skeletal vital effect on oxygen isotope composition (δ¹⁸O) partitions two alternate evolutionary strategies. The first strategy is heavily reliant on a sea water supply chain of CO₂ to supplement respiratory CO_2(met). In contrast, the alternate strategy is less reliant on the sea water supply source, potentially facilitated by increased basal respiration rates and/or a lower photosynthetic demand for CO₂. The comparative vulnerability of these alternative strategies to modern ocean conditions is used to explain the global-wide observation that corals with branching morphologies (and thin tissue layers) are generally more thermally sensitive than corals with massive morphologies (and thick tissue layers). The life history implications of this new framework are discussed in terms of contrasting fitness drivers and past environmental constraints, which delivers ominous predictions for the viability of thin-tissued branching and plating species during the present human-dominated (“Anthropocene”) era of the Earth System.     

Variation in the structure of epifaunal invertebrate assemblages among coral hosts

The high biodiversity of coral reefs is attributable to the many invertebrate groups which live in symbiotic relationships with other reef organisms, particularly those which associate with the living coral habitat. However, few studies have examined the diversity and community structure of coral-dwelling invertebrates and how they vary among coral species. This study quantified the species richness and composition of animals associated with four common species of branching corals (Acropora nasuta, A. millepora, Pocillopora damicornis, and Seriatopora hystrix) at Lizard Island in the northern Great Barrier Reef. One hundred and seventy-eight nominal species from 12 different phyla were extracted across 50 replicate colonies of each coral host. A single coral colony, approximately 20 cm in diameter, harbored as many as 73 individuals and 24 species. There were substantial differences in invertebrate species composition among coral hosts of different families as well as genera. Twenty-seven species (15% of all taxa collected) were found on only one of the four different coral species, which may potentially indicate some level of specialization among coral hosts. The distinct assemblages on different coral species, and the presence of potential specialists, suggests invertebrate communities will be sensitive to the differential loss of branching coral species resulting from coral reef degradation.     

Morphogenesis of the branching reef coral Madracis mirabilis

Understanding external deciding factors in growth and morphology of reef corals is essential to elucidate the role of corals in marine ecosystems, and to explain their susceptibility to pollution and global climate change. Here, we extend on a previously presented model for simulating the growth and form of a branching coral and we compare the simulated morphologies to three-dimensional (3D) images of the coral species Madracis mirabilis. Simulation experiments and isotope analyses of M. mirabilis skeletons indicate that external gradients of dissolved inorganic carbon (DIC) determine the morphogenesis of branching, phototrophic corals. In the simulations we use a first principle model of accretive growth based on local interactions between the polyps. The only species-specific information in the model is the average size of a polyp. From flow tank and simulation studies it is known that a relatively large stagnant and diffusion dominated region develops within a branching colony. We have used this information by assuming in our model that growth is entirely driven by a diffusion-limited process, where DIC supply represents the limiting factor. With such model constraints it is possible to generate morphologies that are virtually indistinguishable from the 3D images of the actual colonies.     

Spatial dynamics of benthic competition on coral reefs

The community structure of sedentary organisms is largely controlled by the outcome of direct competition for space. Understanding factors defining competitive outcomes among neighbors is thus critical for predicting large-scale changes, such as transitions to alternate states within coral reefs. Using a spatially explicit model, we explored the importance of variation in two spatial properties in benthic dynamics on coral reefs: (1) patterns of herbivory are spatially distinct between fishes and sea urchins and (2) there is wide variation in the areal extent into which different coral species can expand. We reveal that the size-specific, competitive asymmetry of corals versus fleshy algae highlights the significance of spatial patterning of herbivory and of coral growth. Spatial dynamics that alter the demographic importance of coral recruitment and maturation have profound effects on the emergent structure of the reef benthic community. Spatially constrained herbivory (as by sea urchins) is more effective than spatially unconstrained herbivory (as by many fish) at opening space for the time needed for corals to settle and to recruit to the adult population. Further, spatially unconstrained coral growth (as by many branching coral species) reduces the number of recruitment events needed to fill a habitat with coral relative to more spatially constrained growth (as by many massive species). Our model predicts that widespread mortality of branching corals (e.g., Acropora spp) and herbivorous sea urchins (particularly Diadema antillarum) in the Caribbean has greatly reduced the potential for restoration across the region.     

Experimental fragmentation reduces sexual reproductive output by the reef-building coral Pocillopora damicornis

Natural and anthropogenic disturbances may fragment stony reef corals, but few quantitative data exist on the impacts of skeletal fragmentation on sexual reproduction in corals. We experimentally fragmented colonies of the branching coral Pocillopora damicornis and determined the number and size of planula larvae released during one lunar reproductive cycle. Partially fragmented colonies significantly delayed both the onset and peak period of planula release compared with intact control colonies. Most fragments removed from the corals died within 11–18 days, and released few planulae. The total number of planulae released per coral colony varied exponentially with remaining tissue volume, and was significantly lower in damaged versus undamaged colonies. However, the number of planulae produced per unit tissue volume, and planula size, did not vary with damage treatment. We conclude that even partial fragmentation of P. damicornis colonies (<25% of tissue removed) decreases their larval output by reducing reproductive tissue volume. Repeated breakage of corals, such as caused by intensive diving tourism or frequent storms, may lead to substantially reduced sexual reproduction. Therefore, reef management should limit human activities that fracture stony corals and lead to decreases in colony size and reproductive output. Accepted: 2 February 2000     

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.     

Species-specific habitat distribution of coral reef fish assemblages in relation to habitat characteristics in an Okinawan coral reef

We determined the species-specific habitat associations of coral reef fishes and environmental characteristics in an Okinawan coral reef in Japan. We focused on three families (Pomacentridae, Gobiidae and Labridae) and attempted to determine differences in habitat utilization. We selected six sites along the coast of Amitori Bay, from the entrance to the innermost part, in order to cover a wide range of habitat characteristics (exposed habitat, semi-exposed habitat and sheltered habitat). The species diversity of coral assemblages was greater at the exposed and semi-exposed habitats, whereas branching coral mostly covered the sheltered habitat. The environmental factors that determine the species-specific spatial association in fishes differed among families. Both biological characteristics (coral morphology and coral species diversity) and physical characteristics (water depth and wave exposure) affected the spatial association of pomacentrids and gobiids. In contrast, physical characteristics such as substrate complexity and water depth affected the species-specific spatial association of labrid species. Further study is needed to determine the ecological factors that regulate the species-specific habitat preference in Okinawan coral reefs.