Marine Biology Research

ISSN: 1745-1000 (Print) 1745-1019 (Online) Journal homepage: https://www.tandfonline.com/loi/smar20

Coral restoration research and technical developments: what we have learned so far

Makoto Omori

To cite this article: Makoto Omori (2019) Coral restoration research and technical developments: what we have learned so far, Marine Biology Research, 15:7, 377-409, DOI: 10.1080/17451000.2019.1662050 To link to this article: https://doi.org/10.1080/17451000.2019.1662050

Published online: 14 Oct 2019.

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Full Terms & Conditions of access and use can be found at https://www.tandfonline.com/action/journalInformation?journalCode=smar20 MARINE BIOLOGY RESEARCH 2019, VOL. 15, NO. 7, 377–409 https://doi.org/10.1080/17451000.2019.1662050

REVIEW ARTICLE Coral restoration research and technical developments: what we have learned so far

Makoto Omori Akajima Marine Science Laboratory, Zamamison, Okinawa, Japan

ABSTRACT ARTICLE HISTORY Coral reef restoration is not the same as forest restoration as its success is not always guaranteed Received 27 July 2018 because of insufficient knowledge of coral biology. The technology of active restoration has a Accepted 2 June 2019 history of only 40 years or less. In spite of many devices and efforts, restoration is often Published online 14 October hampered by low survivorship of colonies, fragments or sexual propagules. In order to 2019 enhance coral resilience and adaptation in a changing world, many new approaches to coral SUBJECT EDITOR ’ reef restoration are being suggested. However, we wouldn t be able to succeed or achieve Naoko Isomura expected result, i.e. recovery and thriving of the coral reefs, if outplanted coral recruits do not grow well and spawn and successfully fertilize in the sea. The cost to restore a few hectares of KEYWORDS reef is often considerable. More studies are needed to improve the methodology. Contractors Coral; coral reefs; restoration; and practitioners of coral reef restoration projects must have advanced techniques supported transplantation; culture by strong science for successful propagation, rearing, and transplantation/outplantation of corals. This review describes what we have learned so far from research on active coral reef restoration and discusses seven topics that may facilitate successful restoration projects.

Introduction Under these circumstances, the Coral Reef Targeted Research and Capacity Building for Management Although coral reefs occupy only 0.17% of the world Project for the East Asia and Pacific Region, funded ocean area (Smith 1978), they form habitats for by the Global Environment Facility, was established 830,000 multi-cellular species that account for about (2004–2009). The restoration working group of the 30% of all ocean species (Fisher et al. 2015). Coral project, in which the present author participated, reefs support commercial and recreational fisheries, examined the current state of restoration and rehabili- attract tourism, and protect the coastline from tation techniques and tested various applications. erosion. More than 100 million people live in tropical Results of the studies are summarized in a guideline and sub-tropical coastal areas with coral reefs. Globally, (Edwards and Gomez 2007) and a manual (Edwards the economic net benefit from coral reefs has a value of 2010). All members of the working group agreed to US$30 billion yr−1 (Cesar et al. 2003) and almost US − announce the following in these publications: $350,000 yr 1 for the value of the potential services of an average hectare (De Groot et al. 2012). Although restoration can enhance conservation efforts, However, the effects of global warming and local it is a poor second to the preservation of original habi- anthropogenic disturbances such as pollution and tats. With the present state of technology, we cannot overfishing are subjecting reef corals to severe stresses, create fully functional reefs. Before launching a coral transplantation project, we must remove all possible resulting in intensified bleaching, sedimentation, eutro- stressors of denuded reefs. phication, and disease. Approximately 75% of the world’s coral reefs are rated as threatened when local Under the present circumstances, however, the threats are combined with thermal stress, which reflects traditional (passive) conservation method, with or the impacts of rising sea temperature (Burke et al. 2011; without minimal human input, is not enough to stop see also Carpenter et al. 2008). In spite of various counter- coral reef degradation, and the development of novel measures by administrators, scientists, and the general restoration methodologies is strongly desired (Rinkevich public, significant positive results are lacking. 2008, 2014).

CONTACT Makoto Omori [email protected] Akajima Marine Science Laboratory, 179 Aka, Zamamison, Okinawa 901-3311, Japan © 2019 Informa UK Limited, trading as Taylor & Francis Group

Published online 14 Oct 2019 378 M. OMORI

Reef-building corals (zooxanthellae) reproduce sexu- given that transplantation/outplantaion accounts for ally by internal or external fertilization and asexually only a small component of restoration relative to the by budding or fragmentation. Methods for restoration global scale of coral reef destruction, some scientists and/or rehabilitation of coral reefs are composed of two are still dubious about the effectiveness of active techniques based on sexual and asexual propagation. coral restoration. However, if a large number of coral Direct coral transplantation via asexual propagation, recruits could be transplanted/outplanted successfully, where corals (whole colonies or fragments) are taken they will become ‘spawning hubs’ or ‘spawning hot- from donor communities and relocated to the site to spots’ and produce an increasingly large number of be restored, has been practised since the 1980s larvae each year that will enhance the expansion of (Alcala et al. 1982; Precht 2006). At the beginning of coral reefs (Amar and Rinkevich 2007; Horoszowski- the twenty-first century, when concern over the degra- Fridman et al. 2011; Montoya-Maya et al. 2016; dation of coral reefs was high, restoration techniques Zayasu and Suzuki 2019). were modified to incorporate a nursery phase where Restoration with sexually and asexually propagated small coral fragments, obtained asexually, are grown corals has two phases: (1) propagation and nursery- to sizes suitable for subsequent outplantation (Rinke- farming and (2) transplantation/outplantation. While vich 2006). In addition to the asexual means of propa- the first phase has been developed considerably, the gation, methods of rearing and outplanting of sexually second phase includes many areas that require propagated coral were studied at Akajima Marine further study, such as species and site selection for res- Science Laboratory, Okinawa (Omori et al. 2008; Iwao toration, time and size of recruits to be transplanted/ et al. 2010)(Figure 1). Later, this technique was fol- outplanted, and design to maintain genetic diversity lowed and modified in several studies (Villanueva and species composition (Rinkevich 2014). The con- et al. 2012; Omori and Iwao 2014). dition of corals after transplantation/outplantation Restoration projects are being undertaken at various must be monitored periodically for 3–4 years until places. However, the revival and prosperity of coral they mature and begin spawning. reefs over a large area, indicating a recovery of ecologi- In addition to the literatures mentioned above cal services, has not been verified. Furthermore, even if (Edwards and Gomez 2007; Edwards 2010), there are a restoration project was reported as successful, there several useful manuals and reviews on the coral restor- is no standard goal. Therefore, restoration projects ation (e.g. Edwards and Clark 1999; Omori and Fujiwara are criticized for attempts to save face after a destruc- 2004; Rinkevich 2005). Barton et al. (2017) reviewed tive development project and/or ship-grounding. Also, recent developments in coral propagation.

Figure 1. Outplanted Acropora tenuis that was raised from eggs at Akajima Island, Okinawa (5 years old). Courtesy of Akajima Marine Science Laboatory. MARINE BIOLOGY RESEARCH 379

The present paper reviews what we have learned so other causes, for the transplantation. The fragments far from research and projects of active coral restor- in nets or containers are carried by divers or boat ation, and discusses on seven topics that may facilitate without taking them out of the water to the transplan- successful restoration projects. Concluding remarks for tation. The site is cleaned to remove algae and other future coral restoration are presented last. foreign matter by abrasion using wire brush just Note that the author uses the term (coral) restor- before transplantation. Then, the fragments are fas- ation to include both restoration and rehabilitation in tened directly on the seafloor with various ways the present paper. using epoxy putty, masonry nails, stainless wires and cable ties (Okubo 2004). So far, fragments of 2–20 cm long or in diameter have been transplanted. The fol- Techniques using asexual propagation lowings are a review for the ecological and physiologi- So far, most coral restoration studies have used asexual cal results after direct transplantation. propagation techniques using fragments of adult colo- In many cases, the growth rate and survivorship, as nies in combination with various nursery-farming tech- well as the fecundity of directly transplanted fragments, niques. These are relatively less labour-intensive and are lower than those of wild established colonies of the inexpensive compared to sexual propagation tech- same size. This is probably because they directed more niques. However, the techniques use fragments with energy to healing and attachment to the substrate. limited genetic diversity which constrains their opportu- Yap and Gomez (1985) reported that survival and nity of fertilization and resistance to disease and future growth rates of the directly transplanted Acropora stress disturbances (Edwards 2010;Bartonetal.2017). pulchra (Brook, 1891) colonies were considerably less than those of undisturbed controls. Also, Plucer-Rosario and Randall (1987) reported that the growth rates of Direct transplantation Pavona cactus (Forskål, 1775) and three other trans- A coral fragment is defined as a live portion of the colony planted species averaged 50–75% compared to refer- that has become physically separated from the rest of ence colonies (controls). Colony size of storm- the colony (Bothwell 1981; Highsmith 1982). The pro- generated Acropora palmata (Lamarck, 1816) that were duction of new colonies by fragmentation is an impor- transplanted for a restoration project in the British tant mode of reproduction and local distribution Virgin Islands tended to decrease slightly in the first among reef-building corals (Highsmith 1982). three months after being transplanted (Forrester et al. Smith and Hughes (1999) deployed 900 artificially- 2014). Its mortality was higher in the first year after trans- generated fragments of three common corals, Acropora planting than the following year. According to Okubo intermedia (Brook, 1891), A. millepora (Ehrenberg, 1834), et al. (2005, 2007), who investigated survivorship and and A. hyacinthus (Dana, 1846) in reef flat, crest and reproduction of three different fragment sizes (ca. 5, slope habitats and observed survivorship after 17 10, and 20 cm long) of Acropora formosa [now months. Reattachment varied from 0% to 50%, and A. muricata (Linnaeus, 1758)] after direct transplantation, was greatest for larger A. intermedia fragments on the both survivorship and fecundity varied depending on reef flat. It was found that A. intermedia fragments had the fragment size and time of deployment. Survivorship the highest survivorship (32%) compared to 15% for A. after 18 months was 98–100% for the 20 cm, whereas it millepora and 8% for A. hyacinthus. Larger fragments sur- was 29% for the 5 cm. Oocyte development was affected vived substantially better than smaller ones (30% vs. by fragment size and developmental stage of oocytes 8%). Fragments deployed on the reef flat survived when fragmented. In smaller fragments, the oocytes in better than those deployed in other habitats. the early vitellogenesis (yolk formation) stage at the Direct transplantation, where fragments of donor time of fragmentation were resorbed, whereas those in corals are taken and relocated to the site to be restored, the late stage continued developing. The fragments is simple and inexpensive. It is easily carried out with the that spawned had lower growth rate, while those that participation of local people. The method is described in resorbed the oocytes carried at the time of transplan- Okubo (2004) and Gomez et al. (2011), and the actual tation showed higher growth rate, suggesting the transplantation projects have been carried out by, for trade-off between growth and reproduction. Fragments example, Onaka et al. (2013) and dela Cruz et al. (2014). of Acropora nasuta (Dana, 1846) spawned in the first year Coral fragments are collected from the natural reef after direct transplantation, but no gametes were pro- with a wire cutter, underwater scissors, chisel, or duced in the third year, indicating that fragments reallo- hammer. It may be possible to use ‘corals of opportu- cated energy resources and infertility occurred for a nity (COOs)’ i.e. the fragments broken by typhoon or certain period of time (Okubo et al. 2009). 380 M. OMORI

Clark and Edwards (1995) found in the Maldives been inhibited during the warmer time of the year that, because of increased mortality and reduced (Yap and Gomez 1985). growth rate of transplanted colonies of Acropora ‘Translocation’ in the present paper refers to the cytherea (Dana, 1846), A. hyacinthus, and A. humilis rescue of whole colonies that would otherwise be (Dana, 1846), the mean percentage cover of live destroyed or severely damaged by coastal and/or corals on transplanted sites declined over seven underwater development. While the motivation for months and the coral coverage did not recover until translocation differs from that for direct transplan- almost two years after direct transplantation tation, the methods are, in many cases, similar (Fuji- (Edwards and Clark 1999). Garrison and Ward (2012) wara and Omori 2004; Kilbane et al. 2008). Practices attempted a direct transplantation in the Caribbean of translocation projects were reported by, for Sea using COOs of Acropora cervicornis (Lamarck, example, Seguin et al. (2009), Kotb (2016), and ter Hof- 1816), A. palmata, and Porites porites (Pallas, 1766). stede et al. (2016). They assessed the survival of 75 reference colonies and 60 transplanted ones over 12 years. Ultimately, no A. cervicornis were alive, and only 3% of trans- Asexual propagation using nursery-farmed planted and 18% of reference colonies of A. palmata coral fragments were alive. For P. porites, 13% of transplants and 7% of reference colonies were survived. Physical dislodge- To initiate transplantation of a few hectares, it is ment resulted in the loss of 56% of the colonies, necessary to prepare a large number of coral frag- whereas 35% died in place. ments in nursery. Asexual propagation techniques Ecologically sound management of coral transplan- with coral fragments farmed in a nursery has been tation should consider the growth and mortality rates introduced as gardening concept (Rinkevich 2006). of the transplants in relation to their size. Yap et al. This method is described in Shafir et al. (2006, (1998) transplanted Porites cylindrica Dana, 1846 and 2010) and Shafir and Rinkevich (2008a, 2008b), and P. rus (Foskål, 1775) and monitored the growth over the actual restoration projects have been shown in 16 months on a reef in the northwestern Philippines. many papers, for example, Shaish et al. (2008) and They found the growth rate of smaller fragments was Johnson et al. (2011). faster than for larger one. Similar results have been A large number of small fragments clipped from obtained for fragments of A. cervicornis, though small donor colonies are attached to artificial substrata and fragments had the lowest survival (Lirman et al. 2010; kept in a nursery for some period until they grow to Goergen and Gilliam 2018). For small fragments, the a size adequate for outplanting. The wounds by clip- energy storage available for survival is small and they ping heal and the fragments firmly attach to the sub- are easily destroyed by predation and physical disturb- stratum during the farming period. Coral fragments ances. On the other hand, if the fragments are too may be farmed without a substratum (Nedimyer et al. large, they will be easily dislodged by wave action 2011; Mbije et al. 2013; Montoya-Maya et al. 2016). before firm attachment. Soong and Chen (2003) ana- Since the gardening concept was suggested, the lysed the results of transplantation of A. pulchra colo- farming technique have been developed for fragments nies in southern Taiwan. The variables studied were in nurseries in closed seawater facilities such as aquaria the origin and length of the fragments, their new orien- and holding tanks, and in situ conditions in calm seas tation, presence of tissue injury, and position of the (e.g. Shafir et al. 2006, 2010; Rinkevich 2014). Lirman fragment. These variables clearly demonstrated that et al. (2010) reported that the growth rate of nursery- the survival rate of large fragments was much higher farmed A. cervicornis fragments exceeded wild colonies than for small ones, and very small fragments tested in the same region. Using fragments of Pachyseris spe- (e.g. <1 cm) were unsuitable for transplantation as ciosa (Dana, 1846) and Pocillopora damicornis (Lin- they tended to be smothered by algae or were naeus, 1758), Afiq-Rosli et al. (2017) verified the simply lost, perhaps due to predation. Furthermore, positive effect of nursery farming, and showed that this study revealed that the removal of large branches the maximum diameter of the nursery-farmed frag- may render the original colonies infertile or result in ments were 1.8–2.7 times larger than direct transplan- lower fecundity for some years. As a result, they con- tation 11 months after transplantation. Also, dela Cruz cluded that fragments of 4 cm long are best for trans- et al. (2015) compared growth and survival between plantation. Temperature, in addition, appeared to directly transplanted and nursery-farmed nubbins of affect the growth and survival of the transplants. Trans- slow-growing corals Echinopora lamellosa (Esper, plants of A. pulchra in the northern Philippines have 1795) and Merulina scabricula (Dana, 1846) and found MARINE BIOLOGY RESEARCH 381 clear patterns for enhanced growth, survivorship, and covered with live coral tissue within one month and attachment rates in the nursery-farmed fragments. generate new branches after three months (Soong Fragments to be farmed should be collected from and Chen 2003). For corymbose or table-type donor many donor (parent) colonies to ensure a high corals, the fragments should be taken from cutting genetic diversity (Baums 2008). If coral recruits are pro- not the whole periphery but from a fan-like sector. duced from a limited number of donors, they may New branches mostly generate from the cut edge, often be composed of clonal colonies. The use of clon- and the coral becomes round about one year later ally produced recruits for transplanting/ouplanting (Soong and Chen 2003; Higa et al. 2018). It is well causes limited genetic diversity within recipient popu- known among aquarists that, in some species, lations, and thus reduces fertilization rate as they pruning the branch tips causes a fast growth of the mature. This may also reduce the long-term benefits branch (e.g. Lirman et al. 2010). Pruning should be of reef restoration. limited to reduce the damage of the donor colony. In order to prepare a large number of fragments for Epstein et al. (2001) showed in a farm culture of Stylo- coral restoration, two underwater farms with donor phora pistillata (Esper, 1797) that pruning more than colonies (donors of different generation) that are able 10% of a donor colony increased the mortality and to provide many recruits for outplantation were estab- the surviving colonies displayed a reduced reproduc- lished off Onna Village, Okinawa. The donor colonies tive activity. However, in the case of the staghorn were collected from wild colonies and were farmed coral A. cervicornis, up to 75% of the colony could be on top of iron poles 50 cm above the seafloor at a clipped to create recruits without negatively affecting depth of 2–3 m (Higa and Omori 2014; Omori et al. the donor’s survivorship and growth (Lohr et al. 2015; 2016). Currently, over 20,000 donor colonies of 54 see also Lirman et al. 2010). species are kept at the farms (Figure 2). The farms of Many researchers recognize that larger fragments donor colonies become spawning hubs that produce survive better than smaller ones during the nursery millions of larvae by themselves (Zayasu and Shinzato farming, as they are better able to tolerate the effects 2016; Higa et al. 2017). of environmental stress, sedimentation, algal growth, For ornamental massive corals like the genus Euphyl- and fish predation. According to Lirman et al. (2010) lia, Dremel tools fitted with a cutting blade work well to who farmed A. cervicornis in a nursery in the Caribbean shear and divide donor colonies (Borneman and Lowrie Sea, while 13 of the 15 small fragments (2.5 cm) were 2001). In an acroporid coral, the exposed skeletons of dead after 20 days (87% mortality), only two of the 15 the fragments, after pruning, will generally be larger fragments (3.5 cm) experienced complete

Figure 2. Farming of donor corals off Onna Village, Okinawa. Over 20,000 colonies are being farmed. Courtesy of Yoshimi Higa, Onna Village Fishery Cooperation, Okinawa. 382 M. OMORI mortality (13%). Fish predation and sedimentation can PVC. They are being widely adopted in various places. be controlled in an ex situ nursery. Forsman et al. (2006) O’Donnell et al. (2017) compared growth and survivor- farmed small fragments of Porites lobata Dana, 1846 ship of A. cervicornis fragments between the floating and P. compressa Dana, 1846 in aquaria and indicated tree nursery and farming on blocks on the seafloor. that size-specific mortality was reduced by the They found that after 10 months, the colonies on the nursery conditions. floating nursery had grown up to three times faster Various types of coral nursery that vary in structure, than those on the blocks. In order to reduce the cost size, and purpose have been devised (Shafir et al. 2010). of farming, some researchers have developed ‘rope For example, a floating nursery was placed at 6 m nurseries’ and they have yielded promising results. depth (14 m above the seafloor) in Eilat, the Red Sea Fragments of branching coral are inserted into the (Shafir et al. 2006). Ten donor colonies from five rope by temporarily untwisting it at about 10–15 cm branching coral species provided 6813 fragments intervals and the fragments are then slid in between (0.5–3 cm height). The advantage of a floating the strands, allowing the twist of the rope to hold the nursery is that, if it is suspended in mid-water, there fragments in place (Levy et al. 2010). tends to be more water movement around it and this In areas where the setting of a floating nursery is facilitates the washing off of sediment. The depth can difficult due to strong currents and/or seasonal be adjusted seasonally to optimize growth conditions weather conditions, more durable fixed nurseries on such as light and sedimentation. The floating nursery the seafloor may be used. The tray or shelf nurseries can be lowered to avoid excessive irradiation when are mostly set 30–50 cm above the seafloor (Shaish sea temperatures rise during bleaching events. The et al. 2008; Higa et al. 2018). Soong and Chen (2003) continual movement of the nurseries with the waves revealed that light intensity is an important factor is postulated to provide better circulation of nutrients that affects the growth rates of A. pluchra. Growth of and gas exchanges so that coral growth is enhanced the fragments on a fixed nursery at a depth of 5 m (Shafir et al. 2010). Nedimyer et al. (2011) developed exceeded that at 10 m after four months, but the frag- two designs of mid-water floating tree nursery that ments on the 5 m depth were more easily destroyed by provided effective results by increasing coral growth waves than at 10 m depth. and reducing the risk of damage from waves The duration of nursery farming varies depending (Figure 3). The first design used a vinyl chloride resin on the species, fragment size, and ambient conditions (PVC) central column with PVC cross arms, a flotation (e.g. temperature and potential predators). The cost for device, and an anchoring device. The second one farming corals in a nursery may become an important used fibreglass rods for the cross arms instead of factor that limits the farming period, but in general,

Figure 3. Nedimyer’s floating tree nursery. Courtesy of Erich Bartels, Mote Marine Laboratory. MARINE BIOLOGY RESEARCH 383 extended nursery care is a trade-off with lower survival inducing a direct current between two electrodes rates under post-settlement. According to Shafir et al. immersed in saltwater (Hilbertz and Goreau 1996). (2006), the use of a floating nursery in Eilat, the Red The chemical reaction of electrolysis leads to an Sea, for 2 cm tall Acropora eurystoma (Klunzinger, increase in pH near the cathode, shifting the concen- 1879) needed five months to attain about 4 cm. tration gradients of dissolved minerals such as dis- Shafir et al. (2010) recommend outplanting branching solved inorganic carbon (DIC). This DIC around the species at around 7–10 cm diameter and massive, cathode precipitates on the structure as aragonite sub-massive, and encrusting species at around 4–5cm. and brucite, which both increase the structure’s stab- Soong and Chen (2003) indicated that there was no ility with ongoing accretion (Hilbertz 1979). Since phys- difference in fragment performance of farming frag- iological processes for coral skeleton growth involve ments between those set vertically or horizontally. In DIC uptake, the highly concentrated DIC is postulated A. pulchra, the fragments had a higher frequency of to be more readily accessible for uptake by transplanted new branch generation in the ends pointing upward corals (Goreau et al. 2004). Goreau (2014)emphasized than those in the ends facing downward after four that low-voltage direct current trickle charges have months. As far as generating new branches was con- increased the settlement of coral larvae at a much cerned, the original proximity, whether proximal or higher rate than at uncharged control sites, and distal, did not have as much influence as the new orien- increased the growth rate of corals and oysters 2–10 tation (Soong and Chen 2003). On the other hand, a (average 3.2) times faster than controls. However, the recent study compared the effect of three inclinations effectiveness of this method has still not been ade- of nursery table top on fragment survival and growth quately inspected. Many factors such as species, strength (Poquita-Du et al. 2017). The effects were not signifi- of the electrical current, ideal coral fragment size, and cant among four species, except for Pocillopora acuta location for deployment remain undetermined. Lamarck, 1816 in which both survivorship and growth Goreau et al. (2004) reported that the density of were significantly lower on vertical nursery tables. zooxanthella and skeletal growth rates in six major Horoszowski-Fridman and Rinkevich (2016) listed 26 coral genera growing on electrically stimulated coral species that were used in outplantation among 86 ‘Biorock’ reefs in Indonesia were higher than those of species that were farmed in coral nurseries worldwide. control (non-stimulated) corals that were adjacent to At the Onna Village, Okinawa, the fragments of 14 Acro- them. However, growth enhancement of P. cylindrica pora species that were not in the former list were suc- nubbins occurred only during the early stages of the cessfully farmed and outplanted (Omori et al. 2016). electrically stimulated phase (Sabater and Yap 2004). Apart from the above methods for nursery farming According to Borell et al. (2010), who measured the of coral recruits, there is another method that may be effect of the electrochemical method on Acropora used for reef restoration with asexual propagation. It pulchra and A. yongei Veron and Wallace, 1984 for has been revealed that spreading tissue and fusion four months under treatment conditions with a con- among nubbins of genetically identical colonies stant calculated current density of ∼2.8 ± 0.1 A m−2, enhances the growth of tiny corals. Forsman et al. the density of zooxanthella was highest for A. pulchra (2015) demonstrated that growth of small (∼1–3cm2) on the cathode, coincidental with the high growth fragments from the same colony of Orbicella faveolata rate relative to the control. However, the cathode had (Ellis & Sander, 1786), Pseudodiploraia clivosa (Ellis & an adverse effect on A. yongei. Romatzki (2014) exam- Solander, 1786), and P. lobata by isogenic fusion over ined the effect of exposure to an electrical field on frag- artificial substrata was as high as 63, 48, and 23 cm2 ments of the same two species using low current per month, respectively, in terms of area encrusted densities of ∼1.7 and ∼2.4 A m−2 at the cathodic and covered by living tissue. They suggest exploiting surface. He concluded that previous reports of signifi- this nature for production of coral recruits for cantly increased growth rates due to electrical stimu- restoration. lation could not be supported for the species examined. For those who believe that the proposed benefits of the electrochemical methodology meet Electrochemical method the objectives of reef restoration, these techniques A technical approach that aims to provide an ideal sub- should be considered with caution (Romatzki 2014). stratum, firm attachment, and enhanced growth of Upon the criticism, Goreau (2014) reviewed all pub- coral transplants is the so-called electrochemical lished results from properly designed projects and con- method or mineral accretion method. It has been trasted them with those that did not meet his criteria, devised based on the principle of seawater electrolysis, but the explanation has not been verifiable as of yet. 384 M. OMORI

The local current density at the cathodic surface formed larvae (planulae) are released. Broadcasters varies with mineral precipitation on the surface, and usually spawn only once each year, while brooders measurement has been difficult in situ. Therefore, in often reproduce for several consecutive months. Corals the previous experiments, the relationship between may also be either hermaphrodites (polyps produce real current density, at the point that coral fragments both eggs and sperm) or gonochoric (polyps have separ- attached, and growth or survival rate could not be deter- ate sexes). According to Baird et al. (2009), the majority of mined. Kihara et al. (2013a, 2013b) made an apparatus corals studied to date are hermaphroditic broadcast to measure real current density and a cage structure spawners (∼63% of species) while the remaining that provided electricity without an external power species are gonochoric broadcaster (∼22%), hermaphro- source. They discovered the growth of Acropora tenuis ditic brooders (∼8%) or gonochoric brooder (∼7%). (Dana, 1846) was enhanced mostly by a feeble current Sexual propagules can be reared for both broadcasters density of about 0.05 A m−2, but the grows rate was and brooders but, first, accurate information on the much lower than that assumed by Goreau (2014). timing of coral spawning is necessary. In some places, the spawning month and time remain unknown. Fortu- nately, however, at any given location there is a reason- Techniques using sexual propagation able consistency from year to year in terms of the Coral restoration using sexual propagation technique general timing of reproduction at the species and has been developed mainly in Japan (Hatta et al. colony level, so even anecdotal observations can help 2004; Nakamura et al. 2011; Omori & Iwao 2014). to identify the exact spawning times for sampling coral Although this technique, using sexual propagules gametes or planulae (Guest et al. 2010). (sexually derived larvae) resulting from large-scale In some broadcasting species, gonad maturity of the spawning events of highly fecund corals (Harrison colony can be judged by breaking a branch from a and Wallace 1990; Hatta 2005), requires more expertise colony, although this invasive technique is not advisa- technology, labour intensity, and costs than the asexual ble. On the night of spawning, the egg-sperm bundles propagation techniques, it has significant advantages appear in the mouth of the polyps 1–1.5 h before of providing greater genotypic diversity among recruits they are released. Fish around the corals may swim that is likely to improve adaptive and evolutionary excitedly around spawning time and this behaviour potential, and increase resistance to future environ- may be an additional indication of spawning. The mental disturbances, thereby strengthening reef com- bundles may be collected in situ by setting up a munity resilience and recovery rates (Guest et al. funnel-shaped device (bundle collector) over the coral 2014). It has also strong potential for scaling-up restor- colony or ex situ after obtaining fragments from donor ation efforts to larger reefal scales (dela Cruz and Harri- colonies (Omori and Iwao 2014). If a slick forms on the son 2017). sea surface overnight after synchronous spawning and remains until morning, fertilized eggs and embryos can be collected and used to rear coral Cultivation and rearing larvae larvae (Omori and Iwao 2014). For brooders, a larvae- A number of sexual propagules of Acropora tenuis were collecting net has also been devised (Guest et al. grown to sexual maturity and spawned at Akajima 2010; Horoszowski-Fridman et al. 2011). However, Island, Okinawa in 2009, four years after rearing from because it is difficult to ascertain when the coral is eggs (Figure 1). This was the first time for a broadcast ready to release planulae underwater, the ex situ collec- spawning of a sexually-raised scleractinian coral in tion of planulae using an overflow pipe and trapping the field (Omori et al. 2008; Iwao et al. 2010). tank system in aquaria is more successful (Omori and The sexual propagation techniques are described in Iwao 2014). In some species of Acropora and Montipora, Omori and Iwao (2014), and the actural restoration pro- spawning can be induced using hydrogen peroxide jects were shown for by, example, Omori (2005, 2011), (Hayashibara et al. 2004). Although fertilization and sub- Nakamura et al. (2011), Villanueva et al. (2012), and sequent larval development have been confirmed by Chamberland et al. (2015). this method, the treatment may cause damage to the Corals have two reproductive strategies that are coral colonies including secretion of mucus or emission important for larval rearing: broadcast spawning and of zooxanthellae, which may lead the death. As the brooding. Broadcasting species release eggs and degree of damage varies with species and condition sperm into the water column for external fertilization of colonies, careful observation of the status of the and subsequent larval development. In the brooding corals during the processing is recommended. The con- corals, fertilization occurs within the polyp and fully centration of hydrogen peroxide and the length of MARINE BIOLOGY RESEARCH 385 exposure should be adjusted with the corals for suc- nylon-reinforced vinyl fabric floating ponds in the cessful artificial spawning induction (Hatta et al. 2004). sea. Omori et al. (2004) reared >420 × 103 coral larvae Hermaphroditic corals seldom self-fertilize (Heyward (134 larvae l−1) in each pond with a capacity of 4 m3. and Babcock 1986; Willis et al. 1997). Thus, for successful Although the planula larvae of brooders settle soon fertilization gametes from different colonies are after leaving the mother colonies, floating larvae of needed. There is a significant negative relationship broadcasting acroporid take 5–8 days before settle- between fertilization rate and genetic similarity ment at 26–27°C, and some merulinid larvae begin to (Isomura et al. 2013a). Shearer et al. (2009) analysed settle after 2–3 days (Babcock and Heyward 1986; Har- population genetic datasets from four coral species to rison and Wallace 1990; Gleason and Hofmann 2011). assess the minimum number of donor colonies required Metamorphosis of eight species of Acropora including to retain specific proportions of the genetic diversity of A. tenuis initiated on contact with an inductive crustose the population. They indicated that 10 donor colonies coralline alga (CCA) Peyssonnelia sp. or Hydrolithon rein- randomly sampled from the original population would boldii (Weber-van Bosse & Foslie) Foslie, 1909 (Morse retain more than 50% of their allelic diversity. Baums et al. 1996). Ritson-Williams et al. (2010) compared et al. (2013) compared fertilization rates of two-parent settlement rates of larval metamorphosis of Acropora crosses and four-parent batches of Acropora palmata, palmata and A. cervicornis in response to four species and found that the rates differed widely, with two- of CCA and other substrata. The larvae of both corals parent crosses having lower fertilization rates (5–56%) had higher rates of metamorphosis on the top surfaces than four-parent batches (31–87%). Iwao et al. (2014) of Hydrolithon boergesenii (Foslie) Foslie, 1909 and Tita- suggest collecting gamete from six parent colonies for noderma prototypum [now Lithophyllum prototypum production of sexual propagules in order to optimize (Foslie) Foslie, 1905]. the fertilization rates and development of embryos. Acroporid settlement competency can be checked When the bundles are gathered at the surface of the using a few larvae in well culture plates with 10 ml sea- container, the water is stirred with a spatula and gently water and small chips of CCA. The larvae are deter- pipetted with a disposable pipette to separate the eggs mined to be competent for settlement when 50% of from the sperm. The eggs are then collected with a the tested larvae settled (Heyward and Negri 1999; pipette or plastic cup and rinsed with fresh, filtered sea- Boch and Morse 2012). On an experimental scale, the water. Sperm are collected from the opaque residual use of neuropeptide Hym-248 promotes induction of solution after collecting the eggs. They may be separ- settlement and metamorphosis in acroporid larvae, ated using a 100 µm mesh filter. although permanent settlement of larvae is not The fertilization rate of acroporid and merulinid always achieved (Iwao et al. 2002). The time for larvae species peaked (>80%) at a concentration of approxi- to maintain competency and settle on substratum mately 106 sperm ml−1 (optimal concentration) (Oliver also varies by species. For example, A. tenuis maintains and Babcock 1992; Willis et al. 1997; Omori et al. 2001; the ability to settle for more than 20 days, but the com- Nozawa et al. 2015). The gamete contact time is petence of A. nasuta was at its highest for only 1–2 days sufficient for 10–40 min. Fertilization and subsequent after which it declined over two weeks, suggesting larval development will be confirmed with these species-specificdifferences in the windows of opportu- methods. As fresh seawater is important when rearing nity for successful settlement and metamorphosis embryos and planula larvae, the seawater in the con- (Morse et al. 1996). The survival of five coral species tainer must be changed frequently until the larvae including Montastraea magnistellata Chevalier, 1971 develop sufficiently to settle onto a substratum. In [now Favites magnistellata (Milne Edwards & Haime, some cases, UV-treated filtered seawater is used for 1849)] indicated that their maximum larval lifespans larval culture (Guest et al. 2014). In the early stage of ranged from 195 to 244 days, but mortality increased development, the larvae are distributed near the progressively after 100 days (Graham et al. 2008). The surface of water. When the larvae began to scatter in operation of larval settlement on a substratum must water column, they are divided into several rearing be accomplished at the peak of competency. tanks to maintain a suitable low density. Larval rearing When competent larvae are released into a tank con- in aquaria is troublesome due to having to change taining ‘biologically conditioned’ artificial substrata (see water. Omori and Iwao (2014) devised an improved also Section ‘Substrata for the settlement of coral rearing method using a flow-through trapping tank. larvae’), they settle in 1–5 days. Settlement rate varies, Using a large rearing tank (500 l), Shimomura et al. but usually, more than 60% of acroporid larvae would (2002) successfully raised up to 500 larvae l−1 of sea- settle onto substrata within one day if surface of the water. A large number of larvae can be reared in a substrata are well-conditioned and larval density is 386 M. OMORI

100–130 planulae l−1 (Omori and Iwao 2014). Settle- Thus, in general, extremely high post-settlement ment is promoted for 2–3 days by the gentle flow of mortality is a key challenge and potential bottleneck water in a tank. Settlement of A. tenuis larvae was not for coral recruitment. Few data reveal, however, that significantly correlated with light intensity, despite the the mortality of Acropora spat differs among species higher settlement rates observed under light intensities and habitats (Suzuki et al. 2018a, 2018b). Among between 130–170 µmol m−2 s−1 (Yusuf et al. 2019). That three dominant species (A. digitifera, A. tenuis, of Goniastrea retiformis (Lamarck, 1816) and Acropora A. yongei), the survivorship of post-three months was digitifera (Dana, 1846) was positive density-dependent: significantly higher for A. tenuis than for A. digitifera. the relationship was exponential for the Goniastrea but In a separate analysis with three bottle-brush species linear for the Acropora (Doropoulos et al. 2018). Pollock [A. awi (Wallace and Wolstenholme, 1998), A. echinata et al. (2017) reported that for Acropora millepora larvae, (Dana, 1846), and A. subglabra (Brook, 1891)], post- densities ≤0.2 larvae ml−1 maximized larval survival settlement survival was always highest for A. awi. and settlement success in culture tanks while minimiz- These authors consider that low survival of other ing maintenance effort. species was possibly associated with slow growth Mortality during the early period of post-settlement rates during the first seven months, and concluded is considerable. Coral spat on a substratum in the sea that species selection is important for successful coral are easily removed or killed by nibbling of fish and cov- restoration, with A. tenuis being the most viable option. ering with macroalgae and sediments (Vermeij and Suzuki et al. (2012) compared mortality of spat in in Sandin 2008; Trapon et al. 2013). In the Red Sea, situ seeding on artificial substrata using three different three-month-old Stylophora pistillata had 5.0% survivor- larval densities in enclosed bag and found that the ship after one month on the reef (Epstein et al. 2001). number of corals that settled on the high-density In the Philippines, survivorship of one-month-old plates (ca. 0.59 spat cm−2) and the low-density plates Pocillopora damicornis spat was less than 5% after four (ca. 0.07 spat cm−2) became almost identical (0.05– months of deployment and none survived on the reef 1.0 spat cm−2) at one month post-settlement. They after one year (Raymundo and Maypa 2004). That of reported that the density within the range 0.5– A. tenuis spat on tiles was less than 10% during the 1.0 spat cm−2 appeared to be optimal for seeding on sub- first five months after settlement (dela Cruz and Harri- stratum. Omori and Iwao (2014) suggested that the initial son 2017). In Japan, for three-day-old spat of density on a substratum should be 0.5–1.5 spat cm−2 in P. damicornis, survivorship ranged from 0% to 16% order to reduce mortality of the spat and avoid infection after six months (Sato 1985) and for 1–1.5-month-old during the early post-settlement period. spat of five species including Acropora solitaryensis On the other hand, under very high-density con- Veron & Wallace, 1984, survivorship ranged from 0% dition, spat may fuse among genetically identical to 12% after 3–10 months (Nozawa et al. 2006). In the clones or form large chimeras (Raymundo and Maypa Great Barrier Reef, survivorship for Platygyra sinensis 2004; Puill-Stephan et al. 2012; dela Cruz and Harrison (Milne Edwards & Haime, 1849) and Oxypora lacera 2017). Chimeras can develop from the fusion of geneti- (Verrill, 1864) was 0.5% and 3.9% after four months, cally distinct coral embryos and juveniles. The fused respectively (Babcock and Mundy 1996). Early post- spat are larger than other spat of similar age so that settlement mortality of Acropora palmata was 86% they can reach the escape-size threshold and stabilize during the first six months in the sea (Chamberland survivorship faster than small spat. Reduction of size- et al. 2015); the survivorship was 12–49% for 6–9 specific mortality among juvenile corals has been weeks in laboratory (Miller 2014). Mortality pressures shown to result from manipulation of the size by continue to act on coral spat until they reach an micro-colony-fusion (Raymundo and Maypa 2004; escape-size threshold (Doropoulos et al. 2012) when Forsman et al. 2015) and/or nutritional enhancement mortality became significantly reduced. This escape- (Toh et al. 2014). size threshold may differ across species but is around nine months for A. tenuis (dela Cruz and Harrison 2017). Inoculation of zooxanthellae Settlement orientation on experimental substrata influenced the growth rate of coral spat (Babcock and The offspring of many corals (approximately 80% of Mundy 1996). In the first few months after settlement, broadcasting species) acquire symbiotic zooxanthellae mortality was highest on highly sedimented upper horizontally from the natural environment (Baird et al. surface of square tiles, but growth and survivorship 2009). It is essential for them to take in zooxanthella during the following five months became higher on within five to seven days after settlement because a these upper surface than on undersurface. failure to do so may lead to death. Establishing MARINE BIOLOGY RESEARCH 387 symbiosis may be enhanced by inoculation with cul- metamorphosis occur consecutively after stimulation, tured Symbiodinium spp. (Suzuki et al. 2013) or by intro- but they are assumed to be a separate phenomenon ducing giant clam Tridacna spp. or coral fragments from (Omori 2016a). Tebben et al. (2011) isolated and outside to the rearing tank (Petersen et al. 2008) at the characterized the chemical signal from bacteria that time of reseeding or immediately after larval settle- induced larval metamorphosis of A. millepora. Later, ment. This process is easy, although the effectiveness Tebben et al. (2015) also identified two classes of of early uptake of specific symbionts for spat survivor- CCA cell-wall-associated chemical compounds as the ship has not been fully elucidated as of yet. Note the main constituents of settlement-inducing fractions. recent finding of heritable variation in Symbiodinium Gómez-Lemos et al. (2018) proposed that optimal community. Quigley et al. (2018) suggested that the coral settlement is caused by complex synergistic inter- strength of the response of genetic compositions of action between CCA-compounds and the CCA-epiphy- zooxanthellae will depend on estimates of both herit- tic microbial films. If larvae do not sense the epiphytic ability and phonotypic variance. Juvenile coral will microbial films on the substrata, they remain in the turn a yellowish colour when the number of zoox- water column for a long period without settlement, anthellae in the spat increases. even when they are competent to do so. Many coral species associate with specific zoox- Whatever substrata are used, it is essential to con- anthellae. Some of the zooxanthellae are mostly the dition them with CCA and bacteria for a period of innately less heat stress-tolerant, such as ‘clade C’ zoox- time in seawater before attempting larval settlement. anthellae [now the genus Cladocephium LaJeunesse & Conditioning of the substrata can be done in the sea Jeong gen. nov. (LaJeunesse et al. 2018)] in adult or in a flow-through aquarium. The optimal length of corals, and are mostly the more stress-tolerant clade time for conditioning is not fixed, but it is preferably A[Symbiodinium Hansen & Daugbjerg (LaJeunesse four to eight weeks. Webster et al. (2004) found that et al. 2018)] and/or clade D [now Durusdinium LaJeu- two-week-old biofilms induced metamorphosis of nesse gen. nov. (LaJeunesse et al. 2018)] when acquired Acropora microphthalma (Verrill, 1870) in <10% of by juvenile corals (Baker et al. 2004; Abrego et al. 2009; larvae, whereas the metamorphosis rate increased sig- Yamashita et al. 2013, 2014). Suzuki et al. (2013) found nificantly to 41% on an eight-week-old biofilm. The that the early uptake of clade A enhanced post-settle- settlement rate of Favites halicora (Ehrenberg, 1834) ment survival in dark places. Baker et al. (2004) found larvae was 25% on a two-week-old substrata immersed coral containing clade D were more abundant on in the sea, whereas it was 68% on two-month-old sub- reefs after episodes of severe bleaching a mortality. strata (Guest et al. 2010). They proposed that the symbiont changes are a The physical characteristics of the substratum may common feature. However, shifts of Symbiodinim aid in the larval settlement. Some species of Porites types (e.g. from clade C to D) may have negative and Acropora settle even on unconditioned red impacts on a number of coral fitness traits including substrata (Mason et al. 2011). The preferred red sub- growth and fecundity (Jones and Berkelmans 2011). strata had spectra dominated by wavelengths 580– 590 nm that was similar fluorescent emission peaks of CCA, indicating that some larvae may determine Substrata for the settlement of coral larvae settlement with signals of light. Whalan et al. (2015) Various substrata made of scallop shells, concrete, slate, compared the settlement of A. millepora larvae on unglazed ceramic tile, polycarbonate, fibreglass- tiles with surface holes of 400, 700, and 1000 µm reinforced plastic, and steel slag have been used so diameter. The larvae showed a markedly higher far. However, larval settlement choice is highly depen- settlement to surface holes that closely matched dent on external cues, such as crustose coralline algae their width (430 µm). Kihara et al. (2013b) reported (CCA) and bacteria on substrata (Morse et al. 1996; that coral larvae exhibited a greater settlement Heyward and Negri 1999; Negri et al. 2001; Webster affinity for a substratum coated with DIC (see et al. 2004), and is not associated with the substratum Section ‘Electrochemical method’) that provide count- material. Coral larvae prefer to settle on substrata that less minute holes. have been ‘biologically conditioned’ in seawater for a Larval settlement on substratum may be counted period of time. For seven Caribbean corals the CCA T. using fluorescent filters or a blue light that causes prototypum and H. boergesenii facilitated larval settle- settled larvae to fluoresce (Baird et al. 2006; Chamber- ment more than the biofilm control for the broadcast land et al. 2017). spawning corals but not for the majority of the brood- Square tiles are often used as the substratum for ing corals (Ritson-Williams et al. 2016). Settlement and coral spat. They are suitable for experimental work, as 388 M. OMORI the number of spat is easily counted. However, sub- from the scaling-up of restoration programs point of strata for the mass production of sexual propagules view, they are least practical, as they need to be manu- should be evaluated to ensure that they provide ally and individually attached to the seafloor. shelter for the spat for protection and maximize the Chamberland et al. (2015) used clay tripod substrata number of surviving corals per substratum. Holes, for larval settlement. The undersides act as better grooved surfaces or crevices provide spatial refuges refuges for coral settlers. Survival of sexual propagules from incidental grazing or predation of newly settled of 2.5-year-old Acropora palmata was 3.4% after settle- spat by fishes and sea urchins. The unglazed reddish ment. It was much higher than that of the propagules brown ceramic grid substratum (river rehabilitation kept in a land-based nursery (0.5%). Furthermore, tiles) having five rows of 1.5 × 1.5 cm square holes Chamberland et al. (2017) devised two slender tetra- bored along the length and breadth were found to pod-shaped concrete substrata (7.9 and 9.8 cm diam.) be preferable for survival of spat (Nakamura et al. on which coral larvae were settled. The substrata 2011). As water passes through the holes, sedimen- were efficiently deployed by wedging them in reef cre- tation hardly occurs, and the spat are protected from vices, without the need for binding materials. After one predation. According to Nozawa (2008), while all coral year the substrata were either firmly lodged on crevices spat of three coral species including Echinophyllia or cemented to the reef framework by encrusting aspera (Ellis & Solander, 1786) that settled on a plain benthic organisms. Average survival of sexual propa- tile surface died within the first four months at the gules was 9.6%, and 67% of the substrata still har- sea, while that settled in the small crevices 3–4mm boured at least one coral spat. deep survived. He compared survivorship of coral It is not necessary that many corals grow on one spat on substrata with projections at 5, 15, and substratum, if at least one propagule survived and 25 mm intervals for two years in the sea, and found matured. From this point of view, the present author that the survivorship on the 5-mm projections was sig- considers that an individual square tube or rectangular nificantly higher than that in the two larger intervals hollow sections substratum (2.5–4 cm in a side) that (Nozawa 2012). The artificial substrata should be easy can be combined like grid on the floating (or fixed) to handle without causing damage to spat and be nursery (Fisheries Agency 2019; Suzuki, pers. comm.) easy to attach to the reef. Cylindrical substrata such would be ideal (Figure 4). Coral spat are protected as the ‘Coral Peg’ (Omori and Iwao 2009), ‘Coral Plug- from predation, sedimentation, and physical dislodge- in’ (Villanueva et al. 2012), and ‘Coral Settlement ment, yet receive enough light to promote coral Device’ (Okamoto et al. 2008) are used frequently, but growth.

Figure 4. Individual square tube substratum (2.5–4 cm in a side) for coral spats. Courtesy of Go Suzuki, Seikai National Fisheries Research Institute, Okinawa. MARINE BIOLOGY RESEARCH 389

Direct larval seeding each larval-enhancement plot. Most of them grew (16.1 cm mean diam.) and spawned successfully. They Mass larval enhancement by millions of sexually-derived consider that direct seeding of coral larvae may larvae from large-scale mass spawning events of highly become an important option for active reef restoration fecund corals has strong potential for scaling-up restor- where larval supply and recruitment success are limiting. ation efforts to a larger scale. Some researchers including Doropoulos et al. (2019) suggest that harvesting wild the present author attempted in situ direct introduction coral spawn slicks, development in a trailer suction of competent larvae onto denuded reefs (direct larval hopper dredger, and release competent larvae over seeding) as an affordable way of enhancing coral settle- degraded reef are promising approach for industrial- ment, but very high mortality of the post-settlement scale reef restoration. spat always became an impediment to the plan. Early Okada et al. (2016) made a large cylindrical net studies in Western Australia (Heyward et al. 2002)and (4.25 m height, 1.7 m diam.) called a ‘larval cradle’ Okinawa (Omori et al. 2004;Aotaetal.2006)sampled that was set over coral assemblage on the depth less slicks from spawning and used competent coral larvae than 4 m at night when mass coral spawning occurs. in seeding experiments. Heyward et al. (2002)released Nearly 100% fertilization occurred by enclosing Acropora larvae from small (1.8 m diam.) floating gametes. Moreover, larval survival during the moving culture ponds into a floorless mesh tent (1.8 × 1 m) on a stage was more than 90% in the ‘larval cradle’. Their reef area. More than 6500 sexual propagules were idea is that when the larvae commence settling, intro- growing on 6 terracotta tiles (110 × 110 × 10 mm) after duce them over artificial substrata covered by net. The four weeks. Recruitment in the most highly seeded settled spat will then be outplanted directly or reared in areas was 100-fold more than the natural levels of recruit- a nursery (see also Fisheries Agency 2019). They con- ment. However, subsequent survival or growth of the sider their techniques to be affordable ways of enhan- recruits was not monitored. Aota et al. (2006)released cing coral settlement in situ with a significant reduction coral larvae cultured in floating ponds over four X- in labour and cost, but the methods need further devel- shaped concrete blocks (2 m × 2 m) that were covered opment for optimum results. by vinyl nets for five days. One week later 2000–5000 spat were counted on each block, but after 18 months only 34–60 juveniles remained per block. Subsequently, Common techniques relevant for coral in Palau, more than one million ex situ reared larvae of restoration with both asexual and sexual A. digitifera were used as seed on cement tiles on con- means crete ‘Pallet balls’ for 24 h resulting in significantly Transportation higher recruitment compared with unseeded control tiles after five weeks. Monitoring after 30 weeks and Coral embryos can be transported one or two days after ∼13 months showed, however, no significant differences gastrulation. However, the recommended time for trans- in the recruit densities between seeded treatments and port is 3–4 days after fertilization when the larvae are well control (Edwards et al. 2015). Cooper et al. (2014) ciliated and move actively. At this stage, the larvae can seeded larvae of Porites astreoides (Lamarck, 1816) tolerate various stressors. A container with a density of directly onto denuded areas of reef basis in Florida. 2000 larvae l−1 can be moved at ambient temperature They caged the settled spat to enhance early post-settle- over 2–3 days with survivorship >90%. Live larvae have ment, but found low survivorship with <1% after five been sent by air successfully from Okinawa, Japan, to months. public aquariums in Europe (Petersen et al. 2005). In contrast, dela Cruz and Harrison (2017) demon- In the case of short distance transportation of larvae strated that mass larval settlement could rapidly by a ship or diver, a sealed container without an air enhance recruitment and coral recovery. They intro- space is advisable. A collapsible polyethylene container duced ∼400,000 A. tenuis larvae in fine-mesh enclosures (10 or 20 l) is squeezed to release the larvae underwater on each of four larval-enhancement plots (6 × 4 m), cov- by a diver when introducing a large number of larvae ering biologically-conditioned 10 × 10 cm tiles on into an underwater net enclosure in order to enhance degraded reef areas in the northwestern Philippines. larval settlement on substrata (Omori et al. 2004). Initial mean total settlement on the 10 substrata in Fragments or whole colonies of donor coral should larval-enhancement plots was 255 spat, whereas no be transported to land aquaria manually without larvae settled in natural control plots. Recruit survivor- delay. An exposure time of a few minutes has not ship began stabilizing after five months, and after been proven to affect the survival rate, thus it is not − three years a mean of 2.3 colonies m 2 survived within always necessary to keep the corals in a seawater- 390 M. OMORI

filled container for a short distance. However, it is rec- been commonly used for restoration (Omori and ommended that the corals are covered with a wet Okubo 2004; Horoszowski-Fridman and Rinkevich sheet to protect them from wind and direct sunlight. 2016). They naturally recruit well but tend to have a While transporting, avoid touching corals by hand poor survival in response to environmental stress. Frag- and squirting seawater directly onto the corals. For ments of some brooding species such as Pocillopora long distance transportation, seawater-filled container damicornis and Stylophora pistillata have also been trans- is covered to protect corals from direct sunlight, and planted or outplanted (Horoszowski-Fridman et al. 2011; the seawater is changed with fresh seawater every 30 Liñán-Cabello et al. 2011). Although species belonging min by exchanging approximately 80% of its volume to the genera Pavona, Montastrea, Galaxea, Porites, and (Heeger and Sotto 2000). Corals produce a large Heliopora have rarely been used in active restoration amount of mucus when stressed. If mucus remains projects, post-outplanting survival of slow-growing on the coral surface for a long time, it may cause massive species are often better than faster growing further stress and infection by pathogenic organisms. branching species (Omori and Okubo 2004). Nakamura et al. (2011) successfully transported 14 Fragments or colonies are commonly attached or large donor colonies (10–43 cm diam.) from Okinotor- stabilized using masonry nails, steel cables, cable ties, ishima Island to Okinawa, 1100 km away, by ship. The marine epoxy, or other adhesives (Gomez et al. 2010; corals were kept on deck in fibreglass tanks with trans- Goergen and Gilliam 2018). In many cases, at the site parent lids. They were covered with shade nets to of transplantation/outplantation, holes are drilled in reduce the light intensity to one-third, and one-third the surface of the reef basis using a pneumatic drill, of the seawater in the tanks was changed with fresh and the area around each hole is cleaned before seawater from the open sea three times a day. Water attachment. Then, each coral fragments or sexual pro- temperature varied between 22.5°C and 28.4°C. Naka- pagules are plugged into the hole. These attached on mura (per. comm.) also successfully transported reef substrata tend to survive better than unattached sexual propagules on substrata using vinyl bags filled fragments (Lindahl 2003). If the fragments are not with seawater and oxygen within five hours from attached firmly, they may be dislodged by waves or a Akajima to Onna Village, Okinawa. strong current, possibly resulting in a higher physical Fourteen large gravid Acropora hyacinthus colonies dislodgement rate (Garrison and Ward 2012). Care (16–37 cm) were successfully transported by air from should be taken when a fragment is attached, make reefs in Singapore to an aquarium in London with a the contact area between the living polyps and reef travel time of ∼34 h (Craggs et al. 2018). The ‘inverted basis as large as possible. Check attachment of all submersion method’ (Delbeek 2008) in which the corals within one day after the transplantation/ corals are attached to a Styrofoam® and suspended outplantation. upside down in the transportation bags, was used. Small fragments and nubbins are taken from donor The initial water temperature in these bags were colonies using a wire cutter and kept in the water tank 27.5°C. The UV filtered seawater was buffered with on land. The fragments are then dried for a minute, sodium bicarbonate to ensure the colonies remained attached to artificial substrata often using cyanoacry- healthy throughout their travel time. late gel, and returned to the water (Shafir and Rinke- vich 2008b). Note there is a report that cyanoacrylate glue showed highly rate of in situ detachment (Dizon Transplantation and outplantation et al. 2008). Goergen and Gilliam (2018) showed that In the present paper, the author defines direct transplan- fragments of Acropora cervicornis attached directly tation as ‘transplantation/transplanting’ and transference with cement pucks and epoxy (marine epoxy?) resulted of nursery-farmed coral fragments and sexual propagules in higher mortality (missing) than those with nails and mainly attached on artificial substrata as ‘outplantation/ cable ties. Marine epoxy is composed of a resin and a outplanting’. ‘Translocation’ refers transference of whole hardener. As the chemical reaction between the two colonies from one part of reef to another in order to parts does not occur until they are mixed, they are rescue them from underwater construction or other inevi- mixed immediately before an underwater application. table reason. In order to maintain stability in the restored Usually the marine epoxy cures in 24 h and adhere coral reefs over the long-term, transplantation/outplanta- less readily to both coral and substratum when tion should be designed so that the corals develop in applied underwater (Dizon et al. 2008). Note the close to a natural condition as much as possible. length of time that the marine epoxy remains workable So far, fast-growing branching corals like those and the hardening time may differ by manufacturer belonging to the genera Acropora and Montipora have and water temperature. Care should be taken to MARINE BIOLOGY RESEARCH 391 completely cover the dead skeletal part of the initial opportunity’ using the coral clustering technique, in polyp in the epoxy; otherwise the new tissue may which several fragments were jointed using plastic grow like an umbrella and take a long time to bond straps, and found 95.5% survival over 270 days. The sur- to the substratum. By pushing the fragment into the vival of fragments was 89% with the ordinary tech- epoxy, the newly formed polyps will all attached to nique, in which fragments were placed evenly on the the substratum (Osinga et al. 2012). Boch and Morse seafloor. Using two staghorn coral species (Acropora (2012) transplanted fragments (<5 cm in long) of Acro- intermedia and A. pulchra) dela Cruz et al. (2014) com- pora digitifera in Tygon tubes and attached to the reef pared the effect of density of fragments between 1.6 substrata via zip ties and push mounts. and 3.1 corals m−2 and revealed after 19 months that Only a few studies have indicated what type of artifi- the growth rate in the high-density was higher than cial substratum is the best for fragment attachment the low-density treatment. On the other hand, and how much time it takes for the fragment to self- Goergen and Gilliam (2018) concluded that survival attach to the substratum. Okubo (2003) compared rate of A. cervicornis fragments transplanted at low the self-attachment rates of 10 cm long Acropora density (0.25 coral m−2) showed significantly higher tenuis fragments stabilized with cable ties on concrete survival and lower prevalence of disease than at high blocks, unglazed ceramic tiles, coral rocks, and iron density (6.25 corals m−2). plates. After two months, about 90% of the fragments Cross-fertilization is the dominant mating pattern had self-attached to concrete blocks, and 50% attached in scleractinian corals (Heyward and Babcock 1986). to unglazed ceramic tiles and coral rocks. However, To enhance fertilization of coral recruits after only 29% attached to iron plates and they were dis- transplantation/outplantation, a number of them lodged when the plates became rusty. Aragocrete- from different clones have to be transplanted close sand molded substrata (Aragocrete 2013), clam shells together so their gametes fertilized at a high rate (Dizon et al. 2008), and iron-steel slag (Mohammed when they spawned. Omori et al. (2016) outplanted et al. 2012) have also been used. In a recent coral coral fragments of a species 60 cm apart (2.8 corals reef restoration project in Okinawa (Omori et al. m−2) in order to enhance fertilization. Because the 2016), asexually-propagated fragments of Acropora sperm rapidly disperse after released from egg-sperm were attached to substrata made of Mug White® (a bundle, the expected fertilizable distance was patented soil hardening agent, Fujimori and Kobori assumed less than 2 m, estimated by numerical simu- 2000). The Mug White® is inexpensive and easier to lation using a sperm diffusion coefficient. The fertiliz- process than concrete plates. Fragments of acroporid able area (sperm concentration > 105 ml−1) could be corals mostly self-attached to the substrata within maintained for more than 20 min when nine colonies two weeks to one month. distributed at 2 m intervals spawned simultaneously Time taken for attachment of coral fragments to (Iwao et al., unpublished data; Okinawa Prefecture substrata may vary depending on the species, season, Government 2017). and fragment size. Experiments were carried out to The coral recruits are best transplanted/outplanted determine the self-attachment time of 12 scleractinian at a site near a native reef. If the site is far from the and one non-scleractinian coral species to natural native site, choose a location with similar environ- calcium carbonate substrata, i.e. dead giant mental conditions and similar coral species compo- clam shells (Guest et al. 2009). Fragments of A. digitifera sition to that of the native site. Coral fragments or and A. hyacinthus showed a faster self-attachment time sexual propagules are fixed to convex surfaces of compared to other species; their median time to 100% coral limestone outcrops. Because the movement of attachment was 16 days. On the other hand, the self- sand and gravel easily damages corals on a flat attachment time of E. lamellosa was longest; their seafloor, avoid the lower parts of the reef basis where median time to 100% attachment was 167 days. the surface is smooth. Placement of the corals to the Concerning the orientation of a coral’s attachment side or top surface of a knoll at least 50 cm above the to a substratum, Okubo et al. (2005) indicated that seafloor is recommended (Higa et al. 2018). the survival rate of vertically attached fragments of Although the growth rate of transplanted/out- Acropora formosa and A. hyacinthus (right angle to planted corals is higher in the summer compared to the ordinary orientation for the species) was higher the winter (Latypov 2006; Piniak and Brown 2008), than horizontally attached fragments after four the action during high sea temperatures and immedi- months. ately before the stormy season should generally be Liñán-Cabello et al. (2011) transplanted 10–15 cm avoided to minimize the risk of bleaching and death long fragments of Pocillopora spp. from ‘corals of (Yap and Gomez 1985; Omori and Iwao 2014). 392 M. OMORI

Effect of various environmental factors on light (underwater high-frequency light fluctuations growth and survival of corals resulting from the lens effect on the water surface) may strongly influence endosymbiont photosynthesis The growth rate and survivorship of various corals trans- of corals inhabiting shallow reef habitats, especially planted/outplanted at different locations differ con- during periods of strong solar irradiance and high- siderably for different species and environmental water temperature. Nakamura et al. (2011) could conditions. Coral fragments or sexual propagules trans- enhance survivorship of sexual propagules in an ex planted/outplanted in poor environmental condition do situ nursery using a natural light and shading by a not grow and survive well. Sites and season for trans- 30% attenuation shade net set during the period from plantation/outplantation must be chosen carefully. For June to November in Okinawa. instance, if the sites are exposed to wave action, a signifi- Blue or white light promotes more coral skeletal cant proportion of coral fragments may be lost during growth than green or red light. In the culture of Monti- storms (Birkeland et al. 1979; Clark and Edwards 1995). pora verrucosa (Lamarck, 1816) and Pocillopora damicor- Alcala et al. (1982) reported a 60% mortality of trans- nis, blue light increased the total amount of chlorophyll a plants at 1.2–1.5 m depth at a relatively exposed site of the coral-zooxanthellae association (Kinzie et al. 1984). over one year. The survival rate of nine coral species Wijgerde et al. (2014) investigated the individual and transplanted on a high-energy reef flat in the Maldives combined effects of blue and red light on the health ranged from 50% to 95% after two years (Edwards and and zooxanthellae density of Stylophora pistillata over Clark 1999). Corals have species-specific conditions for six weeks, and found that blue light resulted in the optimal growth. According to Forsman et al. (2012), highest survival rate, whereas red light negatively Porites compressa thrived at the highest light levels affected the health, survival, and symbiont density. with low flow, while Montipora capitata Dana, 1846 When keeping ornamental corals in aquaria, practical exhibited bleaching and reduced growth in the same sources of light provision include metal halides, light- conditions and grew best in shaded treatments. For emitting diodes (LED), and light-emitting plasma (LEP). rearing sexual propagules, as well as nursery farming Wijgerde et al. (2012) compared the effectiveness of of coral fragments, care must be taken to do with the LED and LEP on the growth of Galaxea fascicularis (Lin- most suitable environmental conditions. naeus, 1767), and found while both light sources were suitable, LEP lighting yielded higher growth rates at higher irradiance levels. Light In order to maintain coral health and achieve maximum Feeding growth, sufficient photons of wave lengths between 400 and 700 nm must be supplied (Osinga et al. None of scleractinian corals are documented to exhibit 2011). The supply of light is not an issue if corals are complete autotrophy. Heterotrophy provides essential reared in the sea at an appropriate depth that suits organic nutrients necessary for coral growth and devel- them. However, if light is not supplied sufficiently to opment (Osinga et al. 2011;Goldberg2018). The corals zooxanthellae symbionts within the coral body, the are known as mesozooplankton predators, and most growth rate of corals becomes reduced. Strömgren employ tentacle capture. They are capable of acquiring (1987) studied the relationship between growth rate nutrition from particulate and dissolved organic matter, and irradiation at different depths for Acropora although the degree of reliance on these sources gener- pulchra off Phuket, Thailand, and found a significant ally has not been established (Goldberg 2018). Some linear relationship between irradiance and length artificial (engineered) foods resulted in a significant grown, with a saturating level at 300–400 W m−2. Yap increase in growth in Montipora capitata Dana, 1846, et al. (1998) also studied the effect of depth and light but not in P. compressa (Forsman et al. 2012). The result intensity on two coral species, Porites cylindrica and suggests that M. capitata may be more heterotrophic P. rus, and found that their growth was influenced than P. compressa. In the case of coral rearing in greatly by the light. The light demand of coral is variable aquaria, food either as a living diet or artificial food among species. An excess of photons may result in should always be provided. In the laboratory, Petersen photo-inhibition or shrinking of the chloroplasts, et al. (2008) fed early juvenile Acropora tenuis daily with which subsequently lowers the photosynthetic capacity freshly hatched brine shrimp Artemia salina (Linnaeus, of zooxanthellae. Care should be taken to avoid an 1758), the micro algae Phaeodactylum tricornutum excessive supply of light intensity to the zooxanthellae. Bohlin, 1897 or a commercially available dry food at Nakamura and Yamasaki (2008) stated that flickering various concentrations. According to them, both MARINE BIOLOGY RESEARCH 393 growth and survival rates of the corals were highest in the transplanted at two locations, and demonstrated that the Artemia nauplii treatment. Juveniles of both Acropora weight after a period of ∼18 months was higher at a reef millepora and A. nobilis digested Artemia nauplii comple- with a mean flow rate of 5.4 cm s−1 than at a reef with a tely after two hours under both light and dark conditions mean flow rate of 4.7 cm s−1. A similar result was (Kuanui et al. 2016). Tagliafico et al. (2018) estimated the obtained for the growth of sexual propagules of Acropora maximum feeding rate of A. millepora for Artemia nauplii hyacinthus. They considered that current was an impor- was 4.6 inds cm−2 h−1 and the concentration to reach tant factor that influences coral growth because the sea- the maximum levels of feeding was above 50 nauplii water flow enhances the flux of nitrogen-rich nutrients ml−1.Tohetal.(2014) found the growth of Pocillopora from the inner lagoon and removes metabolic waste damicornis fed Artemia nauplii twice a week for 24 through tidal exchanges. weeks was enhanced in an ex situ coral nursery. Fed According to Dennison and Barnes (1988), net corals grew significantly faster than unfed ones, with a photosynthesis and respiration were significantly growth rate of 10.7 mm3 week−1 when Artemia nauplii reduced (≈25% lower) when Acropora formosa was (3600 inds l−1) were provided. Osinga et al. (2012)also reared in unstirred conditions compared with stirred fed P. damicornis with Artemia nauplii, the rotifer Bran- conditions. They compared the rates of water chionus sp., and the marine diatom Tetraselmis suecica motion measured in the field with those in the labora- (Kylin) Butcher, 1959, and concluded that Artemia was tory and indicated that coral growth and reef develop- the best food to maximize growth at the lowest cost. ment were influenced by the metabolic responses of Some commercially available artificial dry food may corals to water motion over and around coral reefs. provide a good supplemental diet for juvenile corals, To study the effect of water flow on coral growth, G. but its effectiveness has not been determined because fascicularis nubbins were exposed to four different the ingredients are not always clearly presented. flow regimes (0, 10, 20, and 25 cm s−1, bidirectional Conlan et al. (2018)evaluatedtheefficacy of Artemia flow) for 42 weeks (Schutter et al. 2010). An absence nauplii and artificial foods against unfiltered seawater of flow resulted in significantly lower growth rates, treatment in nubbins (∼6 cm) of adult A. millepora and while the rates were highest at 25 cm s−1.These Posillopora acuta Lamarck, 1816, and found that, authors suggested that higher flow rates reduced whereas P. acuta grew well with Artemia nauplii, the chance of growth disturbance by competing A. millepora showed significantly positive weight gain algae or cyanobacteria, allowing the corals to grow in response to the natural unfiltered seawater. Shafir more readily at a maximum specificgrowthrate et al. (2006) reported a marked increase in the growth under the given environmental conditions. of branching coral fragments farmed in floating nursery Water flow influences coral bleaching. In the 1998 adjacent to an aquaculture cage for the gilthead seab- mass bleaching event in Okinawa, some locations ream Sparus aurata (Linnaeus, 1758). They concluded experienced 100% coral mortality while other nearby that the added growth was due to additional nutrients locations suffered little. Nakamura and van Woesik in the form of dissolved organic matter from food waste. (2001) provided experimental evidence for high survi- vorship of A. digitifera colonies that were subjected to both high sea surface temperatures (SSTs; ranging Water flow from 26.22°C to 33.65°C) and high-water flow (50– The water movement over a reef is responsible to trans- 70 cm s−1), while corals that were subjected to high port the necessarily nutrients, increase particle capture SSTs and low-water flow (2–3cms−1) showed low sur- (Sebens and Johnson 1991), flush the waste products, vivorship. They suggest that spatial differences in coral and enhance photosynthesis and respiration (Mass mortality during the 1998 bleaching event may have et al. 2010). The Hawaiian reef coral Pocillopora mean- been, in part, the result of differences in water-flow drina Dana, 1846 is restricted to turbulent environments, rates that induced differential rates of passive whereas P. damicornis is most abundant on semi-pro- diffusion, which varied among habitats. Water flow tected reefs, and Montipora verrucosa (Lamarck, 1846) is also facilitated recovery from bleaching in the coral Sty- characteristic of very calm environments. Jokiel (1978) lophora pistillata (Nakamura et al. 2003). concluded that the growth, mortality, and reproductive rate of these coral species are influenced by water Suspended particulate matter and sediments motion differently, by controlling the rate of exchange of material across the interface between the seawater Coastal coral reefs are exposed to increasing nutrient, and the coral tissue. In Palau, Boch and Morse (2012) sediment, and pollutant loads that are discharged compared mean fragment weights of Acropora digitifera from land. Terrestrial runoff containing large amounts 394 M. OMORI of suspended sediments and nutrients may have the 2001; Quan-Young and Espinoza-Avalos 2006). following effects: (1) enrichment with particulate According to Suzuki et al. (2018a), shading by macro- organic matter greatly contributes to nutrient avail- algae had a negative effect only on the growth of ability for the propagation of benthic algae and phyto- coral spat and not on their survivorship. Coral spat plankton, and this may have a negative effect on coral are easily smothered by fouling organisms such as physiology and the balance between corals and their ascidians and bryozoans. They can be crashed by symbiotic zooxanthellae (Koop et al. 2001); (2) light the sea urchin Diadema and nibbled by parrotfish reduction due to turbidity reduces the growth rate of (Scaridae). There are over 160 species including corals (Hunter and Evans 1995); and (3) contamination fishes, annelids, crustaceans, echinoderms, and mol- of suspended particles from natural resuspension luscs that consume living coral (Rotjan and Lewis events and dredging activities limits coral sperm avail- 2008). Rotjan and Lewis (2008) provide a comprehen- ability (Ricardo et al. 2016) and inhibit larval settlement sive description of known corallivores, their foraging (Fabricius 2005; Perez et al. 2014). Laboratory and field modes, and coral consumption rates. Although it is experiments were carried out to determine the effect of desirable to rear corals in an environment where suspended sediments on fertilization, larval survival, such corallivores and fouling organisms are absent, and settlement in A. digitifera (Gilmour 1999). Both this is not possible in the sea. high (≃100 mg l−1) and low (≃50 mg l−1) levels of sus- At the Akajima Marine Science Laboratory, Okinawa, pended sediments significantly decreased fertilization, sexual propagules of corals were reared with algae- although the lower level was not exceptionally high grazing juvenile top shell snails Trochus niloticus (Lin- even under natural conditions. Gilmour (1999) con- naeus, 1767) in a nursery cage suspended in the sea sidered that the introduction of an additional stress (Omori 2005; Omori and Iwao 2014). Grazing trails of in the form of high levels of suspended sediments young T. niloticus (5–10 mm in basal shell diameter) coupled with a naturally high variability in recruitment were practically harmless to the coral spat (Tamura may have had a considerable effect on the successful 2008). Toh et al. (2013) reported that grazing by the supply and settlement of coral larvae to a reef. sea urchin Salmacis sphaeroides (Linnaeus, 1758) and Naturally, a location where seawater contains rich gastropod Trochus maculatus (Linnaeus, 1758) was suspended particulate matter is not suitable for coral also effective in controlling macroalgal fouling in rearing, farming, and outplanting. Even lower sediment rearing tanks of sexual propagules. The biocontrol of loads affect the survival of newly settled coral spat of A. fouling organisms in nursery reduces labour expendi- hyacinthus and Leptastrea purpurea (Dana, 1846) within ture because the manual removal of unwanted organ- the first 2–4 weeks post-settlement. Moeller et al. isms is no longer needed. Although many sea urchins (2017) concluded that co-occurrence of moderate sedi- are grazers, care should be taken in species selection mentation events during and immediately after for biocontrol because some are known to damage periods of coral spawning could reduce recruitment small corals (Forsman et al. 2006). In a large flow- success substantially. Humanes et al. (2017) revealed through nursery tank, young rabbitfish Siganus spp., that survivorship of juvenile A. millepora was strongly butterfly fish Chaetodon kleniie (Bloch, 1790), and sur- reduced with a high concentration of suspended sedi- geonfish Acanthurus triostegus (Linnaeus, 1758) were ments (∼100 mg l−1). Acropora tenuis and Pocillopora introduced to remove macroalgae and sea anemones acuta juveniles survived, but their growth was (Nakamura et al. 2011). reduced to less than half or to zero, respectively. Baria et al. (2010) examined the effect of herbivore Omija (1987) developed a convenient method for exclusion on the survival of six-week-old A. tenuis spat measuring suspended particles in sea sediment and showed that the survival was significantly higher (SPSS). He reported that SPSS in Acropora dominated in the caged treatment than uncaged treatment coral reefs was less than 10∼30 kg m−3 after studying (33.0% vs. 4.7%) after three months. In order to the relationship between coral reef resilience and avoid nibbling damage by scarid fish and the SPSS off the Ryukyu Islands, Japan (Omija 2004). barred filefish Cantherhines dumerilii (Hollard, 1854) after outplanting, protective cage placement over the corals has been attempted (Omori and Iwao Macroalgae, fouling organisms and protection 2014). According to the preliminary experiments, of corals from predation by invertebrates and macroalgae sometimes grew inside the cages, inter- fish fering with coral growth. Therefore, the cages had Competition for space and light between coral spat to be removed within one year in order to allow and macroalgae is well documented (e.g. Lirman grazing fish to remove the algae. MARINE BIOLOGY RESEARCH 395

Application of population genetics concluded that larval recruitment by sexual reproduc- information for coral restoration tion is important to maintain population densities, and sexually produced seedlings with 15 colonies are Artificially-restored coral reefs should be as similar to sufficient to produce adequate genetic diversity, at natural reefs as possible. This is one of the most impor- least for the next generation (Zayasu and Suzuki 2019). tant tasks for a restoration project and it ensures the Naturally, different genotypes of a species differ in restored coral reefs are able to persist for a long time. growth and other characteristics. Lirman et al. (2014) For this, the natural condition of local reefs such as found, based on more than 1700 nursery-farmed A. cer- species composition and genetic characteristics must vicornis fragments and colonies from 37 distinct geno- be studied before a restoration project starts. Further- types (identified using microsatellites) in Florida and more, the project should be designed keeping in mind the Dominican Republic, that fast-growing genotypes that genetic and species diversities are maintained grew up to an order of magnitude faster than slow- and that genetic disturbance does not occur. Since the growing genotypes. Algal-symbiont identity showed development of molecular tools, we now know that a that clade A was the dominant symbiont zooxanthellae coral reef may be composed of populations of a for all coral genotypes, except for three clade C-domi- different genotype. Larval exchange is more locally nated genotypes having similar growth rates. and regionally restricted than previously thought. Because of that, distribution expansion is slow and recovery may be retarded (Vollmer and Palumbi 2006; Costs and benefits Zayasu et al. 2016). For example, populations of a repre- sentative Caribbean coral Acropora palmata are divided Edwards and Clark (1999) suggested, based on their into two sub-regions. They have experienced little or no experience of coral transplanting activities in the Mald- recent genetic exchange between the western and the ives, that one should, where possible, let natural eastern Caribbean. Puerto Rico is identified as an area of recruitment drive recovery. Ferse et al. (2013) con- mixing between them (Baums et al. 2005). Even a cluded that, in the presence of detrimental environ- species inhabiting the same place may show differences mental conditions, coral transplantation in North in growth rate and tolerance to environmental stress Surawesi, Indonesia, may not be an effective method depending on the genotype. Another Caribbean coral to boost coral recruitment. Instead, they recommend Acropora cervicornis has four different genotypes that the provision of a stable substrate for larval settlement differ in growth rate under the same environmental con- combined with improved management to reduce ditions (O’Donnell et al. 2017). chronic stressors. Activities for stabilization of the Concerns expressed by respondents regarding seafloor, setting structure, and construction of artificial genetic modifications to wild populations include the reefs to enhance the settlement of coral larvae (e.g. Fox possibility of establishing monoclonal populations et al. 2005; Fox and Haisfield 2010; Williams et al. 2019) that would reduce fertilization success or artificially may be included as another strategy for coral restor- increase the local dominance of certain genotypes ation. One or two strategies should be chosen, so that may depress the genetic contribution of wild gen- that the largest effectiveness will be achieved with otypes (Young et al. 2012). Previous restoration pro- the least cost. jects and experiments proceeded largely without The cost required for the restoration of a few hectares considering the genetic factors. Today, goal is to of reef is often considerable. In order to carry out a coral promote an effective restoration by knowing the geno- restoration project aimed to restore the ecological type of the donor colonies and coral propagules service of coral reefs, a great number of coral fragments (Baums 2008; Schopmeyer et al. 2012). and sexual propagules are needed. The ‘success’ of the According to Zayasu et al. (2016) who studied the project has been mostly assessed as the number of trans- genetic diversity of Acropora tenuis in the Nansei planted/outplanted fragments with little information Islands area, Japan, there was no clone in the wild about their growth and survival (e.g. Guzman 1991; population, suggesting that the propagation of this Lindahl 1998). However, the ‘success’ should be species mainly takes place sexually in the wild. There judged, with a reasonable cost, when outplanted frag- are more than two regional populations where the ments or sexual propagules increased the number and genetic exchange is partially restricted; indicating colony size more than the initial condition when all that artificial movement of coral colonies between mature sexually. Omori (2016b) suggested that a coral different regional populations is not preferable. In survival rate of more than 40% at 3–4 years post-trans- genetic study of Acropora yongei in Okinawa, it was plantation/outplantation would be a reasonable 396 M. OMORI performance target for active coral restoration. This sur- Edwards et al. (2010) estimated a product of fragmen- vivorship benchmark was proposed temporarily based tation costs somewhere between US$1.4 and $1.9. In on the result of coral reef restoration project in fact, however, as not all fragments and/or sexual pro- Okinawa (Higa et al. 2018). The average initial fragment pagules survive after outplantation, the cost for coral size of three Acropora species [A. cytherea, A. tenuis, restoration with the matured colonies will further and A. valenciennesi (Milne Edwards, 1860)] was 5.4– increase. The cost of a single 2.5-year-old Acropora 10.3 cm geometric mean diameter (GMD) when out- millepora grown from a sexual propagule on the reef planted. After three years they would grew to 22– costs at least US$61 (Guest et al. 2014). By improving 46 cm GMD and all mature sexually. If the survival rates early survival rates during the nursery-rearing phase, a are maintained at 40%, their coverage area would six-month-old outplanted colony of Acropora valida become 3.2–14.0 times greater than the initial condition. (Dana, 1846) could be produced for about US$11.2 The cost for coral reef restoration varies from around (Villanueva et al. 2012). Based on restoration exper- US$10,000 to 50,000,000 ha−1 (Spurgeon 2001). iment of Acropora palmata in Curaçao reef, Chamber- Whether the cost is reasonable or not may be deter- land et al. (2015) estimated that keeping one RSU in mined by the economic benefits of coral reefs. For land-based nursery for 2.5 years costs US$325, of instance, the economic value of Hawaiian coral reefs which 79% covered the operational costs of the is estimated to be US$9.7 billion (US$878 ha−1 nursery, whereas, RSU reared on the reef for 2.5 annually) (Cesar and van Beukering 2004), whereas years costs US$13. In the meantime, the total pro- that of Tubbataha Reef, the Philippines, is US$6 duction cost for direct seeding of mass-cultured million (US$17 ha−1 annually) (Subade 2007). coral larvae in the northwestern Philippines was US The framework for computing cost of reef restor- $1654 (dela Cruz and Harrison 2017). This equates to ation is provided by Edwards et al. (2010) based on a production cost of US$20.94 for each of the 79 colo- asexually produced transplants. Modifications were nies surviving after 35 months. made in Villanueva et al. (2012)tofit with sexual propa- More recently, assumptions of cost and benefits to gation. The operation cost is expressed as man × hour, evaluate two large-scale reef restoration approaches regardless of the location because labour costs differ using a trailer suction hopper dredger was attempted depending on the country. The cost for transplantation by Doropoulos et al. (2019). They compared the har- varies significantly according to the method and local vesting, development, and release of wild coral condition. For instance, in the case of an in situ spawn slicks onto a target reef, with transplantation nursery, the distance from the harbour and depth of of gravid coral colonies to provide a seed the nursery are factors that influence the cost. population and local source of larvae. Comparisons Published costs of production and nursery farming incorporate the best available information on demo- for one fragment or one substratum containing at graphic rates to estimate population growth, begin- least one sexual propagule [‘recruit-substrate unit ning at embryo production to colony maturity four (RSU)’, Chamberland et al. 2015] are shown in years following deployment. They estimated that the Table 1. Currently, the costs of the sexual propagation median cost of 4-year-old mature corals was cheapest vary from US$5.3 to US$163. This is in sharp contrast using the slick harvesting approach at US$55 per to the asexual propagation techniques that a single colony, whereas, it was US$206 for the transplantation fragment costs from US$0.15 to US$13.2 (Table 1). approach.

Table 1. Costs (USD) of production, nursery farming, outplanting, and monitoring for one fragment and one substratum containing at least one sexual propagule (RSU). Project Location Method Production/nursery farming Transplant/outplanting Monitoring dela Cruz et al. (2014) Philippines Direct transplantation $0.15–0.37 Heeger and Sutto (2000) Philippines Asexual, nursery farming $1.00 Shafir et al. (2006) Israel Asexual, nursery farming $0.5–1.0 Higa et al. (2018) Japan Asexual, nursery farming $9.80 $3.35 $2.60 Nakamura et al. (2011) Japan Sexual propagation $163.0* Villanueva et al. (2012) Philippines Sexual propagation $4.40 $0.87 Omori and Iwao (2014) Palau Sexual propagation $5.00 $1.30 Guest et al. (2014) Philippines Sexual propagation $29.0** Chamberland et al. (2015) Curaçao Sexual propagation $5.42* $1.57*** *Cost for RSU. **Cost including outplanting. ***Cost including monitoring. MARINE BIOLOGY RESEARCH 397

The current technology using sexual propagation differ from each other. Are their life shorter than sexu- can be further developed or refined to maximize the ally propagated corals? production and minimize the cost. So far, extended Ecological factors of coral reefs differ considerably nursery care is a trade-off with lower rates of survival depending on location. Species and method of restor- under rapid post-outplanting. Certainly, if farming in ation should be chosen to be the best to the location. the nursery could be shortened and survivorship of Based on the landscape restoration concept, if the after outplanting improved, an individual cost of transplanted/outplanted fragments or sexual propa- sexual propagule or RSU in the long term, may gules grow and succession occurs, natural recruitment, approach the cost of the asexual counterparts. Manu- as well as the natural introduction of reef fish and ally attaching substrata with settled corals to the reef mobile invertebrates, will be expected. Choice of is both time-consuming and expensive. Chamberland coral species and the best place to transplant/outplant et al. (2017) presented a novel approach whereby are the most important factors for success of active res- coral spat settled on small tetrapod-shaped concrete toration projects. For prediction of dispersion and substrata that were placed on the reef without the settlement of coral larvae, physical observations and need for manual attachment. The time required for out- simulation of advection and diffusion are necessary. planting was reduced considerably; these authors Ladd et al. (2018) emphasize importance of incorporat- showed a 5–18 fold reduction in outplanting cost of ing ecological processes such as predation, herbivory, Acropora palmata compared to common methods. and nutrient cycle that facilitate coral restoration. Okubo and Onuma (2010, 2015) argued, from eco- They also gave special consideration to the operationa- logical and economic points of view, for reforming lization of density-dependent theory in its relevance to transplantation efforts using mixture of asexually pro- growth and survival of transplanted corals, and cross- pagated and sexually propagated coral recruits. Based fertilization of gametes released in the water column. on the few reports where an analysis on cost-effective- Furthermore, Doropoulos and Babcock (2018) advocate ness was possible, Bayraktarov et al. (2016) concluded examination of metapopulational connectivity in coral that the most cost-effective coral reef restoration pro- restoration planning. jects in a developing country were direct transplan- Coral restoration can only be an effective manage- tation, estimated at US$11,717 ha−1. In contrast, the ment tool if it is cost-effective. In developing countries least cost-effective approach for coral reef restoration where tourism and fishing industry are largely depen- was one that used a combination of a stabilizing sub- dent on coral reefs, direct transplantation or outplant- strate and transplantation of fragments, estimated at ing of nursery-farmed fragments, in which local US$2,879,773 ha−1. residents can participate, will be continued (Heeger et al. 2001). However, the cost to restore a few hectares of coral reefs is often considerable. Contractors and Concluding remarks for future coral practitioners must use advanced techniques supported restoration by science for coral propagation and transplantation/ The purpose of coral restoration is the recovery of coral outplantation. Regardless the scale of restoration reefs and enhancement of biodiversity and ecological project, the project should be carried out following services provided by coral reefs. Its aims are to increase the advice of knowledgeable experts. New coral restor- coral coverage, development of coral spawning hubs ation will be preceded by a training workshop and/or for larval dispersion, and maintenance of genetic and lectures offered by experts. In most cases, coral restor- species diversity. However, techniques of coral restor- ation activities are designed and supported with the ation are still in an early phase. The mortality rate assistance of national or local agencies, and oversight during the early post-settlement stage of juvenile of the restoration activities is crucial to prevent the corals is high, and loss of transplanted/outplanted misuse of funds. As the support for coral restoration corals (both fragments and sexual propagules) before project grows, the next step will be documentation of maturation is considerable. More investigation of benchmarks that can be used by administrators and coral husbandry is required in order to overcome the practitioners to determine the efficacy of the efforts bottleneck of large post-settlement mortality. Many and impacts of the activities. studies have found that both colony size and polyp For asexual propagation method with nursery age influence fecundity (e.g. Kojis and Quinn 1985; farming, it is preferable to first establish large nursery Okubo et al. 2007). Further studies are needed to farms of donor colonies with various species collected answer the question whether the length of lifetime of from larger reef area (Figure 2). Small coral colonies or asexually propagated fragments of different donors storm-generated ‘corals of opportunity (COOs)’ 398 M. OMORI collected from neighbouring natural reefs are being cannot help improving the techniques. It is necessary adopted throughout the Philippine (Feliciano et al. to provide science-based benchmarks that can be 2018). However, collection of a large number of COOs used by restoration projects to evaluate successes for coral transplantation is not easy in many pauperized and challenges of efforts, and to make modifications areas. In addition, COOs contain many clonal fragments where needed. The present author has proposed that yielding a nursery population with much lesser genoty- the goal of coral restoration should be the survival pic diversity than desired. A good design for transplan- rates of more than 40% of outplanted recruits at their tation/outplantation is needed, so that fragments and maturation and spawning (Omori 2016b). For restor- sexual propagules are able to maintain high genetic ation of Acropora cervicornis, Schopmeyer et al. (2017) diversity and produce numerous larvae that extend propose the benchmarks for the first year of activities: over a wide area. To enhance fertilization by trans- >80% survivorship of nursery corals and >70% of out- planted or outplanted corals, the fragments and planted corals. sexual propagules should be placed close enough to In reef restoration projects, growth and survival of ensure high fertilization rates. The recruits should be coral recruits, as well as the scale of restoration, are carefully arranged to minimize the possibility of two most widely used indicators of restoration success. clonal corals being placed adjacent to each other According to Hein et al. (2017), among 83 works of (Omori et al. 2016). Coral gene-banks of donor colonies coral transplantation/outplantation projects that they and coral recruits may be established to help research- referred, the mean duration of monitoring was less ers to find strains that have higher growth and survivor- than two years and the majority were for one year ship and more resilience to environmental disturbance. or less. However, monitoring after one year is ineffec- Because of many advantages over the asexual tual for restoration effectiveness (Hein et al. 2017). propagation methods, in particular for maintaining Natural reef recovery can be a lengthy process genetic diversity, application of sexual propagation ranging from five years to decades (Connell et al. techniques are increasing as an approach for reef res- 1997; Gilmour et al. 2013). Considerations are necess- toration (Nakamura et al. 2011; Omori and Iwao 2014; ary for the evaluation of restoration initiatives to the Chamberland et al. 2015; dela Cruz and Harrison continuous and sustainable delivery of ecosystem ser- 2017). However, rearing sexual propagules ex situ and vices that are inherently linked to the long-term outplantation still require tedious handling and is success of a restoration project (Schrack et al. 2012; time-consuming. More studies are needed to improve cited by Hein et al. 2017). the cost-effectiveness and to reduce the operational In order to enhance coral resilience and adaptation costs. Direct larval seeding may be a promising option. in a changing world, many new approaches to coral To the best of the author’s knowledge, the largest reef restoration are being suggested and devised (e.g. scale coral restoration projects were those of Costa van Oppen et al. 2017; Rinkevich 2019), and some Rica, in which 7.1 ha were restored using 85,000 frag- have been tested primarily in the laboratory. Some ments (Guzman 1994; cited by Edwards and Clark unexperienced researchers may consider that restor- 1999) and Bali, Indonesia, in which one ha was directly ation is not technically difficult. However, coral reef res- transplanted with about 112,000 fragments (Onaka toration is not the same as forest restoration as its et al. 2013). During the Coral Reef Conservation and success is not always guaranteed because of insuffi- Rehabilitation Project of Okinawa Prefecture, Japan, cient development of the technology. We wouldn’t about 120,000 nursery-farmed fragments were out- be able to succeed or achieve expected result, i.e. planted in 3.12 ha off Onna Village, Okinawa, over six recovery and thriving of the coral reefs, if trans- years from 2010 to 2016 (Okinawa Prefecture Govern- planted/outplanted coral recruits do not grow well ment 2017). A further larger scale outplanting project and spawn and successfully fertilize in the sea. is planned by the Mote Marine Laboratory and It is important that principles and information in ter- Nature Conservancy in Florida, USA (Mote Marine Lab- restrial conservation biology and ecology are applied oratory and Aquarium 2019). to coral restoration measures and techniques. Further So far, over 300,000 coral fragments and colonies development of techniques is expected through com- were transplanted, translocated or outplanted in munication among the scientific community, the Okinawa, Japan. Some of them were performed by public and private aquaria, and the ornamental aquar- private sectors. According to limited data available, ists (Leal et al. 2014). Some aquarists recognize that however, the survival rates of post-transplantation are maintenance of water quality for rearing fast-growing less than 40% before maturation. And, as many cases Acropora species is more difficult than other species. of failure have not been studied, these experiences In order to maintain a high level of regional species MARINE BIOLOGY RESEARCH 399 diversity, the propagation and outplantation tech- (2015) aimed to cross-breed corals that have survived niques for slow-growing but strong and long-lived, massive bleaching events and track the resilience of massive and encrusting species should also be devel- the offspring. Hybridization of Acropora sometimes oped so that they are adopted for coral restoration occurs in nature (e.g. Willis et al. 2006; Isomura (Muko and Iwasa 2011a, 2011b). et al. 2013b). Occasionally, this increases genetic At present the most prominent problems for coral diversity and makes novel genetic combinations that reef conservation may be global warming and ocean may be beneficial for adaptation. For example, acidification (e.g. Bruno and Valdivia 2016). Both hybrids offspring group of Acropora loripes (Brook, genetic fitness and acclimatization may play impor- 1892) × A. tenuis tolerated warmer, more acidic tant roles in boosting heat tolerance (Barshis et al. water than pure bred A. tenuis, with survival rate 2013; Palumbi et al. 2014). Several researchers are ∼16–34% higher (Chan et al. 2018). If the hybrids trying to identify ‘super corals’ that possess an are comparatively resilient in elevated temperature, inherent physiological tolerance to environmental the interspecific hybridization may be combined stress in particular locations, such as the Red Sea, with sexual propagation techniques. However, many the Persian Gulf, and Samoa Island (Barshis et al. attentions are needed to be directed towards investi- 2013; Krueger et al. 2017). Quigley et al. (2018) high- gating fundamental aspects of ecological benefits and lights the importance of inheriting a genetic architec- risks, such as quantifying trade-offs in growth and ture for regulating genetic composition of symbiont thermal tolerance. zooxanthellae, that is flexible enough to respond to ‘Super corals’ may be found over a wide area and it changing environmental conditions. These people may not be necessary to search a particular location. An consider that juvenile survival may promote popu- example is thermally resilient A. tenuis that was reared lation replenishment to build reef resilience. Once in Yomitan Village in Okinawa (Figure 5). The Scleracti- such maternal-line genotypes are identified, they nia that formed the largest part of coral reef structures could be used in targeted selection programs to appeared in the Triassic period of the Mesozoic era, i.e. produce high-quality brood stock for restoring ca. 240 million years ago (Romano and Palumbi 1996). degraded reefs (Drury et al. 2017). Further work During such a long history of evolution, the corals must should focus on identifying host genotypes that cor- have gained genes to tolerate the various environ- relate with stress-tolerant host phenotypes and ident- mental stresses encountered. Thus, there may be ify the mechanisms driving high survival of particular small populations (genotypes) that maintain physio- coral cohorts (Quigley et al. 2018). van Oppen et al. logical resilience to such extreme conditions of heat

Figure 5. Two reared genotypes of Acropora tenuis at Yomitan, Okinawa. The left coral has been bleached by high temperature while the right one showed the thermal tolerance. Courtesy of Kouji Kinjo, SeaSeed Co., Okinawa. 400 M. OMORI and ocean acidification. It has been reported that coral Aota T, Shibata S, Watanuki A. 2006. Development of coral populations that bleached once have adapted and/or reef restoration technology; mass culture, transportation – acclimatized to thermal stress (Guest et al. 2012; Pratch- and settlement of coral larvae. Midoriishi. (17):4 10. Japanese. ett et al. 2013), suggesting that such hidden genotypes Aragocrete. 2013. Aragocrete: DIY live rock. Reef News. appear after the heavy bleaching of a normal [Accessed 2013 Aug 19]. http://www.reef2reef.com/ams/ population. aragocrete-diy-live-rock.96/. Proposals may occur to farm a narrow subset of gen- Babcock RC, Heyward AJ. 1986. 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