Degradation and restoration of coral reefs

Marine Biology Research, 2011; 7: 3
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INVITED REVIEW

Degradation and restoration of coral reefs: Experience in Okinawa, Japan

MAKOTO OMORI* Akajima Marine Science Laboratory, Zamamison, Okinawa, Japan

Abstract Coral reefs in Okinawa, Japan, have declined due mostly to human pressures. There are still possiblities to restore coral reefs locally by amelioration or removal of the local chronic stressors. Political support, scientific information, and the will of local stakeholders are crucial for successful amelioration. Development of techniques for restoration by artificial efforts such as underwater silviculture and transplantation are definitely required. Coral propagules for transplantation may be cultured by either of two approaches: asexual or sexual propagation. The rehabilitation of coral reefs by means of asexual propagation is simple and less labour-intensive compared to sexual techniques. However, most of the transplanted pieces share the donors’ limited DNA, giving the reef a smaller gene pool. On the other hand, sexual propagation may result in genetically more diverse corals, but is labour-intensive and more expensive. Both techniques require devices for rearing after transplantation. This will become one of the key areas of research in the near future. Some 4-year-old colonies of Acropora tenuis, cultured from eggs and transplanted to the seabed at Akajima, Okinawa, had grown to 20
25 cm in diameter and initially spawned in June 2009. This indicated the possibility of using this technique to assist local coral reef restoration. Although the small scale of success so far may not be significant, given the wide range of degradation of coral reefs, certain methods of rehabilitation have proved promising enough to continue our endeavour.

Key words: Coral, coral reefs, culture, rearing, restoration, transplantation

Introduction Despite increasing attention and conservation management measures taken by scientists, nongovernmental organizations (NGOs), the public and government agencies, coral reefs are declining continuously due to human pressures. In the IndoPacific, the average annual coral cover loss was about 1% during the 20 years before 2003 with 2% between 1997 and 2003 (Bruno & Selig 2007). According to Wilkinson (2008), 19% of the world’s coral reefs have been destroyed and show no immediate prospects of recovery, and a further 15% are under imminent risk of collapse within 10
20 years. The situation is similar around Okinawa (the waters in Okinawa Prefecture), Japan, where rich coral reefs used to exist. Corals reefs around the populous Okinawa Island and Ishigaki Island have particularly degraded in the last 40 years (Figure 1).

To emphasize how important it is to protect coral reef ecosystems, some scientists have attempted to quantify their socio-economic values. Contemplating the death of species, there are ethics and moral considerations that are difficult to quantify, and although it would not be right to make restoration decisions based purely on economic values, those estimates may act as a trigger to save some coral reefs from degradation. Cesar et al. (2003) estimated the economic value of goods and services provided by coral reefs of the world to be roughly US$29.8 billion per year. They estimated the potential net benefit from the coral reefs of Japan (i.e. Okinawa) to be US$1665 million per year. What can we do to save corals from dying? We must reduce stresses leading to degradation, and try to rehabilitate coral reefs. Driven by such aspirations, Akajima Marine Science Laboratory (AMSL) is now advocating for the reduction of degradation

*Correspondence: M. Omori, Akajima Marine Science Laboratory (AMSL), 179 Aka Zamamison, Shimajiri-gun, Okinawa, Japan 9013311. E-mail: [email protected] Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway, and the Marine Biological Laboratory, University of Copenhagen, Denmark

(Accepted 18 January 2010; Published online 30 September 2010) ISSN 1745-1000 print/ISSN 1745-1019 online # 2010 Taylor & Francis DOI: 10.1080/17451001003642317

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M. Omori and excessive use of coral reefs by tourism are also causes of the degradation. Ocean acidification (Hoegh-Guldberg et al. 2007) is something for the future and not a current impact, although press coverage about this may act as a warning to society. Coral bleaching

Figure 1. Coral cover decline in Okinawa Island after 1972. After the return of administrative rights over Okinawa to Japan in 1972, rough-and-ready economic development proceeded, and it caused mismanagement of public works. Coastal reclamation, red soil run-off, coral bleaching, eutrophication, and outbreaks of the crown-of-thorn starfish have been causing the most serious impacts to coral reefs in Okinawa Island. The figure was drawn based on various data sources including Sakai & Nishihira (1998) and Nakaya (2001).

caused by human behaviour and developing techniques for mass culture of corals for restoration of the reefs. Akajima Island where the laboratory is located is one of the Kerama island groups located 40 km west of Okinawa Island. The present review relates the main causes of coral reef degradation in Okinawa and describes various approaches for restoration of coral reefs mainly in Okinawa. It also presents recent technical developments at Akajima and perspectives concerning culture and transplantation of corals.

Significant coral bleaching events occurred from 1997 to 1998 worldwide during a strong El Nin˜o (Hoegh-Guldberg 1999). In Okinawa Island, bleaching has been attributed to sea surface temperatures (SSTs) rising and remaining 1
28C higher than the usual average monthly maximum SST for nearly one month in August 1998, the hottest month of the year. The reef-building dominant coral species, such as Acropora and pocilloporid corals, suffered catastrophic damage (Nakano 2004). Loya et al. (2001) reported that species richness and coral cover at Sesoko Island, Okinawa, reduced by 61% and 73%, respectively, between 1997 and 1999. They found that a community-structural shift occurred on the reefs of Okinawa Island, resulting in an increase in the relative abundance of massive and encrusting coral species. The mass coral bleaching occurred at Akajima too, but mortality was relatively low, because the shelf around the Kerama island groups blocked the warm water mass from the Kuroshio currents. Nadaoka et al. (2001) suggested that one of the primary causes of the regional variability of the coral bleaching and consequent mortality in Okinawa was the regional variation of water temperature. The frequency of coral bleaching events in Okinawa has increased since 1980. After 1998, the bleaching events in 2001, 2003 and 2007 saw SSTs rise, but again there was regional variation of coral mortality around Okinawa coasts. The effects of the bleaching on fertility remained after these events, even though the corals recovered. Both the number of oocytes per polyp and the number of testes per polyp of Montipora digitata (Dana, 1845) were significantly less in 1999 after bleaching than in 1996 before bleaching (Hirose & Hidaka 2000). Laboratory fertilization of Acropora in 1999 after bleaching dropped from usual rates (94%) to an average of 42% at a sperm concentration of 105 ml
1, suggesting that production of new coral recruits was reduced greatly after the bleaching (Omori et al. 2001).

Degradation of coral reefs Coral reefs in Okinawa have suffered from coral bleaching, red soil run-off, eutrophication, excessive fisheries, and rampant over-development of land areas, with massive proliferation of concrete structures. Chronic outbreaks of crown-of-thorns starfish

Red soil run-off and eutrophication Many tropical and subtropical islands such as Okinawa contain fine-particle soils termed generally as ‘red soil’ (laterite soils containing high concentrations of iron). Red soil run-off tends to occur when

Degradation and restoration of coral reefs in Okinawa 5 poor land use is combined with natural factors that induce erosion. Because of topographic features in which mountains are steep and rivers are short, and heavy rainfall that is erosive, red soil run-off occurs after human activities that convert rural or mountain greenery into bare land. After the return of administrative rights over Okinawa to Japan in 1972, rough-and-ready public works and economic development proceeded, and they caused mismanagement of reclaimed land and land based construction that still results in red soil run-off. The discharged red soil is deposited on the moat portion of the reef flat, and during typhoons and tropical winds these deposits are resuspended by ocean waves, resulting in turbid seawater. This almost cyclical process of deposition and resuspension causes chronic damage to coral reefs. Larval settlement on the seabed is seriously interrupted; recruits cannot grow, and die. Although a red soil ordinance was enacted for Okinawa in 1995, nearly 40% of the coasts are still subject to the red soil pollution from farmlands (Omija 2004). In addition, fertilizer, agricultural chemicals, and livestock excreta that enters rivers ultimately causes eutrophication in the coastal areas. Many scientists believe that the spread of coral diseases is related to deteriorating water quality, nutrient run-off, and rising SSTs (cf. Kuta & Richardson 2002; Bruno et al. 2007).

Reclamation, land-based construction and tourism Public works, including coastal reclamation, are still a big cause of coral reef destruction in Okinawa. The problem is that once such public works by national or local governments are approved, the management decisions are obstinately executed even many years later, although the social situation and the public’s concern over the environment have changed significantly. Coral reefs should be preserved unless coastal alteration is necessary for peoples’ lives. According to income statistics for Okinawa’s residents, tourism income is the second largest category of revenue from outside the prefecture. Coral reefs are, however, often threatened by excessive use by tourists. The capacity of coral reefs to support tourism, including diving, should be measured and respected, but many users and stakeholders rarely consider the sustainability of the reefs. Figure 2 shows how tourism-related activities are causing disturbances. When diving services and fishermen at Akajima restricted their activities, on their own initiative, at one of the most popular diving spots (Nishihama) for 3 years after the bleaching event, the coral cover significantly increased during the closed period, 1999 to 2001.

Excessive fisheries According to the fishery statistics of Okinawa Prefecture (2008), landings of reef fish such as grouper (Serranidae), parrotfish (Scaridae) and emperor fish (Lutjanidae) declined by 31%, 41% and 14%, compared to those respective species’ landings two decades ago. The collapse of healthy coral reefs under stress destroys almost all their value as a resource for both fisheries and tourism. Although the effect of coastal fisheries on the present condition of coral reefs in Okinawa has not been scientifically studied, it has been pointed out that recent excessive exploitation of coastal fish depletes fish stocks and changes the interaction among fauna and flora in coral reef ecosystems (cf. Bellwood et al. 2004). Reduction of stocks of intermediate-size herbivore fish such as parrotfish may cause expansion of seaweeds and, accordingly, the loss of substrates for attachment of coral recruits and increase of their mortality. Herbivorous sea urchins such as Diadema and Echinometra are, however, abundant in Okinawa. Moreover, the loss of structural complexity by coral decrease that affects the safe space for spawning and protection of reef fish may result in reduction of fish stocks.

Figure 2. Variation of coral cover of two popular diving spots (Kushibaru and Nishihama) at Akajima (modified after Taniguchi 2004). Data are based on 0.530 m belt transect survey. Coral cover (35%) of the two spots in September 1998 indicates condition of corals immediately after a coral bleaching event. Remarkable recovery of the coral reef community occurred from 1998 to 2001 after the coral bleaching at Nishihama when fishermen and diving services, on their own initiative, closed this diving spot for 3 years. After 2001, however, an abnormally high population of crown-of-thorns starfish (COTS) devastated coral reefs in the area until 2006. At Nishihama, the local diving association killed the COTS regularly. The effort seemed to help conservation of the corals in the early period, but ended in failure at a later stage. At Kushibaru where the elimination programme was not taken, the coral cover decreased from 30% to 3% by 2006.

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Crown-of-thorns starfish Predation by the crown-of-thorns starfish (COTS) Acanthaster planci (Linnaeus, 1758) has gained notoriety in Okinawa since 1969 as a threat to coral reef ecosystems. Almost 13 million starfish were removed from the reefs between 1970 and 1983. Despite this intensive effort, costing approximately US$6 million, this control programme is now regarded as unsuccessful, as almost all coral reefs around Okinawa Island have been catastrophically devastated by COTS (Yamaguchi 1986). As a result, drastic changes in the coral reef community occurred. In some places the hard coral community was replaced by a soft coral community or a Sargassum community (Nishihira & Yamazato 1974). The outbreak of COTS has been chronic around the Okinawa area, and recovered coral communities have been affected again and again in recent years. In the waters of Akajima, the outbreaks occurred in 2001 and ended in 2006 when COTS abruptly disappered from the waters. Members of the local diving service association killed about 77,000 individuals of COTS between 2002 and 2006 in their most important sea areas targeted for protection. However, coral coverage of the island’s north coast (Kushibaru) decreased from 30% to 3% (Figure 2). No one knows what causes outbreaks of the COTS. However, some believe that artificial eutrophication creates phytoplankton blooms which provide food to the larvae of COTS and enhance their chances of survival. Others assume that the declining population of predators (fish and shellfish) that feed on the juvenile COTS have also brought about an increase in survivability. It has also been suggested that the previous COTS outbreak in Okinawa was fostered by half-hearted control programmes, which increased the relative food available per COTS, thereby improving conditions for the remaining individuals (Yokochi 2004). It is apparent that COTS escape and that effective control of their population by extermination is impossible in large areas. In Okinawa, it has been suggested that intensive elimination activity in small areas (i.e. 5 ha) can only be effective at regular intervals, even though this approach has not always been successful (Figure 2). Restoration of coral reefs The term ‘restoration’, in environmental parlance, means the act of bringing a degraded ecosystem back into, its original condition, as far as possible (Edwards & Gomez 2007). There are two main strategies for restoring coral reefs. One is restoration

by means of eliminating negative factors in the background environment. Another is restoration by means of artificial efforts, such as substrate stabilization and underwater silviculture of corals. Since human population and activities have increased greatly, it is rarely possible to restore coral reefs to their original state. However, if we could reduce human interferences and maintain the environment in good condition, recovery of corals from damage due to acute disturbance, from natural phenomena or even after predation by COTS, would be rapid. Political support, scientific information and stakeholders’ opinion are crucial for the success. Common reef-building corals such as the genera Acropora and Pocillopora have the capability to grow rapidly and mature early, and reefs can be revived within 5
10 years. Recovery of coral reefs by elimination of negative factors is the minimum necessary for restoration. Unless the chronic stresses are reduced, propagation of corals is retarded, the reef continues to degrade, and active restoration with artificial approaches is futile. In order to proceed with restoration by means of recovery of the environment, academic scientists must gather and quantify data on: (1) cause(s) of local coral reef degradation, as well as the synergistic impacts of stressors; (2) whether these cause(s) and stressors have been removed; and (3) natural and socio-economic factors that obstruct recovery. It is also an important task for scientists to fix clear standards for restoring the environment to a favorable condition. Coral reef restoration projects often proceed without prior indicators, such as the percentage of live coral cover, or even numerical targets for decreasing stressors. Without having agreedupon, quantifiable initial facts and goals, any restoration project may be more vulnerable to political and/or social pressures and thus fail. Monitoring a restoration project for an extended period of time is critical. Without monitoring there is no assurance that a particular project is effective or whether it should or should not be repeated. On the other hand, the term ‘conservation’ is used in the context of efforts to preserve original habitats. Conservation management of coral reefs has adopted the general idea of marine protected areas (MPA). The underlying theory of an MPA is that regulating specific human activities within defined borders enhances the recovery of coral reefs and survivorship of resident organisms. The number and size of MPAs are increasing worldwide. However, a few scientists have pointed out that the great majority of MPAs, particularly those intended to protect coral reefs currently, may fail to meet their management objectives (cf. Jameson et al. 2002); there are many ‘paper parks’, in which MPAs are

Degradation and restoration of coral reefs in Okinawa 7 legislated into existence without measures to change human pressures, due to lack of funds or will. Mora et al. (2006) state that although 18.7% of the world’s coral reef habitats are contained in MPAs, only 1.6% of reef area is within adequately managed MPAs. Most of the MPAs around Okinawa are small and less than a few hundred metres in width, and smallscale fishing activity is often allowed within the protected areas. It may be difficult to enforce large MPAs without fishing zones in Okinawa and Southeast Asian countries, since dense populations include fishermen living in the coastal areas. More discussions are needed between environmentalists, scientists and local stakeholders concerning the size, shape, and network of managed marine areas to ensure a social consensus for conservation and restoration of coral reefs. At Akajima, scientists and stakeholders debate how to restrict diving activity in their surrounding coral reefs including MPAs. I have learned in Okinawa during the last 20 years that grass-roots education of local people, reasonable reparation for fishermen, financial transparency, participation of local leaders in decision making, and maintenance of reliable relationships between the ecological science community and local stakeholders through long-term interactions are keys for the coral reef conservation (Figure 3). Restoration of coral reefs will be achieved not by messages from governments, but by the willingness and enthusiasm of local stakeholders.

Figure 3. Public education activity at Akajima Marine Science Laboratory. The economy of Akajima is largely dependent on tourism. If the coral reefs lost their resilience and beauty, the prosperity of the island could not continue. The laboratory has been offering marine studies for students and publishing a bimonthly newsletter describing coral reefs to local stakeholders. Today, all islanders know how important the coral reefs are.

Rehabilitation of coral reefs by artificial efforts This strategy means efforts to replace equivalent lost habitats by active measures such as the reconstruction of habitats and/or replanting of corals. Rehabilitation of the ecological functions of coral reefs is the goal. It includes artificial improvement and/or creation of coral habitat through civil engineering (physical rehabilitation) and underwater silviculture and transplantation (biological rehabilitation) approaches. In places where the movement of sand, rubble and fragments of dead coral branches injure corals and interfere with a natural process of recruitment, engineered stabilization of the seabed, creation of habitat and regulation of currents with artificial reefs, natural rocks and artificial aquaculture structures have been attempted (Clark & Edwards 1999; Fox & Pet 2001; Omori et al. 2006). Competing ideas among scientists and engineers vary widely, from creating coral habitat with large concrete ‘reef balls’ (Sherman et al. 2002) or wave-dissipating blocks with unevenly processed surfaces (‘Eco-Block’, Maekouchi et al. 2010), to the use of weak electric current on substrata. Settlement of corals has been enhanced on the ‘Eco-Blocks’ installed at Naha Port, Okinawa (see also Fenchel & Uiblein 2011). Depositing CaCO3 onto steel frames by means of low-voltage direct current seems to enhance larval settlement and the growth of corals; several groups have employed the technique (Hilbretz & Goreau 1999; Sabater & Yap 2002; Goreau et al. 2004). However, to date, neither artificial reefs nor electric current has proven to be a very efficient restoration tool when used for transplantation measures or natural recruitment. The efficacy of the electric reef has not yet been dismissed in Okinawa. Remarkable growth of reef-building corals on floating pontoons composed of steel and concrete, which are protected from rust with feeble electric current, has been observed (Kihara et al. 2009). Research is being carried out here to understand the physiological mechanisms that may accelerate the settlement and growth of corals. Many hermatypic corals expand their distribution by sexual reproduction. Fertilized eggs and larvae disperse over wide areas, settle into polyps, and build up colonies by budding or division of polyps. But, when a part of the colony is broken by, for example, typhoon waves, fragments settle on the neighbouring seabed and grow up asexually to form new colonies. Coral propagules for transplantation may also be spread by human action, using either asexual or sexual propagation of corals.

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Table I. Coral cultivation and transplantation. 1. By means of asexual propagation a. Collection of fragments 0Transplant b. Collection of fragments0Trimming/formation0Rearing of propagules in nursery on land or in the sea0Transplant 2. By means of sexual propagation a. Larval settlement onto artificial substrata in the sea (use of natural recruitment of coral polyps)0Transplant b. Collection of slick (embryos) 0Cultivation of larvae0 Seeding to the seabed or onto substrata in the sea c. Collection of sperm/egg bundles0Fertilization 0Cultivation of larvae0Settlement on substrata0Cultivation of polyps (propagules) in land facility or in the sea0Transplant

Technique of rearing and transplantation using asexual propagation of corals At present the techniques are to either (1) affix coral fragments, trimmed from donor colonies, directly to the substrate, or (2) transplant nursery-grown coral pieces (propagules) after letting them grow to a certain size in a nursery (Table I). Successive transplantation of coral pieces collected from nursery-grown fragments may be employed in the latter case. Fragment transplanting involves breaking off pieces of adult coral colony and affixing them elsewhere on the reef. Since the 1990s, this fragmentation technique by means of asexully propagated corals has been attempted in various reefs in Okinawa (cf. Misaki 1998; Nishihira 2007). Accomplishment of the fragment transplantation to rehabilitate degraded coral reefs in Okinawa has not been clear mostly due to lack of long-term monitoring. Limited numbers from the monitoring data indicate that average survivorship of transplanted fragments after 4 years is about 20% due to mortality in the natural processes (Omori & Okubo 2004). The success of coral transplantation varies greatly depending on species, method, site of transplantation, etc. A number of studies have been carried out to discover the best way to increase survival and growth rates of transplanted corals (cf. Epstein et al. 2001; Soong & Chen 2003; Okubo 2004; Rinkevich 2005; Okubo et al. 2007). These studies revealed that: (1) pruning more than 10% of the branches increases mortality of the donor colony; (2) large fragments have much higher probability of survival; (3) very small fragments are unsuitable for transplantation, because they tend to be smothered by algae or get lost, perhaps due to nibbling by fish; (4) the most suitable fragment size of Acropora for transplantation is 4
6 cm in diameter; (5) sexual reproduction varies depending on size of the fragment; (6) fragments are best kept underwater while being transported from sampling site to nursery and

from nursery to transplantation site; (7) firm fixation of the fragments onto raised substrate is critical for survival and growth
if corals are transplanted on unstabilized substrate or flat seabed they may be buried or damaged by material moved by stormdriven waves; and (8) after transplantation, personnel should check colonies regularly and eliminate macroalgae and the coral-eating gastropods Drupella spp. for an extended period of time (minimum 3 years). Using knowledge obtained in Okinawa, a largescale coral transplantation project employing the fragment transplanting technique is being carried out over 1.3 ha on a reef flat at Bali Island, Indonesia (Indonesia/Japan Bali Beach Conservation Project; Onaka et al. 2008). The participants have transplanted about 112,000 coral fragments of Acropora spp. and others taken from the nearby coral reef area onto 12,000 limestone rocks (approx. 1 m 1 m, 0.8 m height each) that were placed on the sandy bottom in 2007 and 2008. The fragments were fixed with the 2-nails/cable-tie method (Okubo et al. 2005). The survival rate after 1.5 years is surprisingly high, at more than 90% (Nishihira & Prasetyo, personal communication). It should be noted, however, that such a successful transplantation is only possible in waters where seawater quality is favourable for corals, coral cover near the transplantation site is dense, and damage caused by predation and nibbling of invertebrates and fishes is small. Rinkevich (1995) and others (cf. Shafir & Rinkevich 2008; Shaish et al. 2008) recently proposed ‘gardening the coral reef concept’ that is based on a two-step protocol: (1) rearing coral propagules in nurseries to plantable size, and (2) transplanting the nursery-grown coral colonies. They developed a rearing technique for small fragments including nubbins (minute portions of a coral colony or a coral fragment containing only a few polyps) in specially designed nurseries, and they emphatically state that only the establishment of large-scale nurseries and transplantation action will be able to cope with extensive reef degradation on the global scale. So far, however, the second step, i.e. transplantation of nursery-grown coral colonies, has not shown promise. Rehabilitation practices that use a limited number of donor colonies may reduce gene flow among restored coral reef populations. The asexual method of propagation shares the donors’ limited DNA, giving the reef a smaller gene pool. Also, collection of large numbers of coral fragments may injure the donor colonies and communities.

Degradation and restoration of coral reefs in Okinawa 9 Techniques of culture and transplantion using sexual propagation of corals Corals are highly fecund, thus larval rearing has the potential to produce large numbers of juvenile corals (propagules). A technique for culturing sexually propagated corals and transplantation has been developed at Akajima (AMSL) (Hatta et al. 2004; Omori 2005, 2008). Corals may broadcast gametes for external fertilization or internally for brood larvae. At present, artificial larval culture for reef restoration is concentrated on the genus Acropora, a few members of the family Faviidae and on brooders such as the genus Pocillopora. The sexual propagation approach may result in genetically more diverse corals, but is labour-intensive and more expensive than the asexual propagation approach. In order to obtain coral gametes or fertilized eggs, accurate information on the timing of coral spawning is critical. Cultivation of corals from eggs can be attempted either by using larvae collected from surface aggregates (slicks) after mass spawning or by laboratory fertilization. If spawn slicks are utilized, then natural levels of genetic variation can be attained without collecting sperm/egg bundles from donor colonies. The embryos and larvae are then bred in the laboratory or in floating ponds in situ until larvae (planulae) are able to settle to the bottom. Cultured planulae can be used for restoration in two main ways: (1) they may be released directly onto the seabed of degraded reefs or artificial reefs at very high densities and allowed to settle naturally, or (2) they may be settled onto artificial substrata and reared in aquaria or in situ nurseries until they are ready to be transplanted to degraded reefs (Table I). Seeding should be done when larvae are at the peak of competency for settlement, which will vary depending on species. Mesh enclosures may be used for seeding in the sea. A technique that combined floating larval rearing ponds with direct seeding has been tried in Western Australia and Okinawa (Heyward et al. 2002; Omori et al. 2004). The results have shown that early recruitment can be significantly enhanced; however, the majority of these settled corals died due to natural processes. Therefore, at present, this method is not favoured as a reef rehabilitation technique until positive evidence of a long-term effect has been demonstrated. The coral planulae may settle on materials such as concrete, ceramic or terracotta tiles. However, conditioning of the substrata is essential before attempting larval settlement because larvae follow special chemical signals emitted by certain bacteria and coralline algae on the substrata (cf. Morse et al.

1996). They settle well onto substrata that have been placed on the seabed a month or more beforehand, allowing coralline algae and bacterial films to grow on the surface. The larvae metamorphose into polyps (juvenile corals) after settlement. Juvenile corals are then cultured in aquaria or in situ nurseries until they are ready to be out-planted. Concurrently, algae-eating juvenile top-shell snails Trochus niloticus Linnaeus, 1767 are released into nurseries so that algae do not smother the corals on the substrata. In late 2006, 18 months after egg culture, colonies of Acropora tenuis (Dana, 1846) had grown to an average 5.8 cm in diameter in cages suspended in the sea; they were then transplanted experimentally onto the seabed near Akajima (Omori et al. 2008). In June 2009, some of these 4-year-old colonies, as well as 5-year-old ones, had grown to 20
25 cm in diameter (Figure 4) and spawned initially, showing the possibility of using this technique to assist coral reef restoration (Iwao et al. 2010). An alternative sexual propagation technique in Okinawa, which does not require cultivation of larvae, is to allow coral larvae to settle naturally onto specially designed portable coral settlement substrata deployed in areas just before coral mass spawning. The substrata that receive high recruit densities are thereafter reared in that spot or transplanted onto degraded reefs (Okamoto et al. 2008). This technique is very simple, but the portable substrata must be situated at the exact time and place where dense populations of recruits are available. Again, mortality may be very high due to natural processes. Considerable research is

Figure 4. Cultured Acropora tenuis at Akajima, Okinawa. The coral propagules were cultured from eggs in the nursery starting in June 2005 and transplanted onto seabed at Akajima in December 2006. They spawned in June 2009, the first time in their life. The photograph was taken in January 2010 (4.5-years old; about 25 cm in diameter).

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needed before this technique is used in applied restoration efforts. Feasibility of coral reef rehabilitation It is humbling and somewhat depressing to compare the small scales of active restoration projects relative to the worldwide scale of reef degradation. Discouragement is possible, given the small efforts to save reefs that stretch as far as the eye can see. Also, there is no guarantee that a particular degraded ecosystem will return to its original condition in a few years, although the rehabilitation of the natural ecosystem can be controlled somewhat. However, if we could restore coral reefs locally in many places, then the function of coral reef ecosystems could be preserved, eggs and larvae of corals could be supplied to neighbouring areas, and cascade benefits into the future. Also, the formation of complex three-dimensional structures of corals and the colonization by multiple coexisting species (Nishihira 1993) may increase species diversity of the reefs gradually over a time scale of years. Currently, the general public are in favour of transplantation of coral fragments on the reefs in Okinawa and participate in the process and it is often reported in the media as an activity for environmental preservation. It has a good public image as does terrestrial reforestation, and the participants enjoy such events for transplantation, although activity by unskilled divers may sometimes damage reefs unintentionally. Saving coral reefs is not something that we can do in two or three years, but perhaps in a decade. In order to evaluate whether a coral reef has been rehabilitated, it is necessary to continue longterm monitoring on the transplanted corals at regular intervals until the corals grow and spawn normally. There are doubts about the efficacy of rehabilitation of coral reefs by underwater silviculure and transplantation; regrettably, we have to admit that our techniques are still in an experimental stage. Also, we must keep in mind that the present artificial approaches and technological novelties should not be used as an excuse for permitting coastal reclamation, or as substitutes for more important efforts towards reduction of stresses caused by human interference. There are a number of hurdles in restoration technology that we must overcome. Establishment of coral propagules at nurseries in the sea is often obstructed by competition with other invertebrates such as sponges and tunicates. Physical factors such as current, light and temperature that affect survival and growth of transplanted corals have not been adequately studied. Nibbling and predation by fishes and coral-eating gastropods on newly transplanted corals can be a serious problem,

although the risk varies with location. Rearing coral colonies after transplantation will become one of the key areas of research in coral reef restoration in the near future. Although coral reefs may be held in public trust by governmental agencies, the cost of rehabilitation should be offset by the benefits gained. This is not an easy burden for artificial restoration to overcome, since restoration may not show uniform outcomes. Estimates derived from nursery-grown fragments suggest that US$0.5
1.0 is needed per propagule (Shafir et al. 2006). At a spacing of 1 m on a degraded reef, this would suggest culture costs alone of US$5000
10,000 per hectare (for the 10,000 propagules/ha that would be needed) and labour costs for underwater transplantation of about US$25,000 (5 persons 100 h). The price of a nursery-grown coral colony is US$3
5 in Indonesia. AMSL’s methods of culturing corals by sexual propagation are more expensive and labour-intensive. The cost of one propagule (ca. 6 cm in diameter) would be US$10. Development of techniques for coral reef restoration became one of Japan’s fisheries national projects since 2006, and accordingly the Fishery Agency has established Akajima Coral Hatchery (ACH) at Akajima. As a part of the research there, a few large coral colonies were successfully transported from Okinotorishima, Japan’s southernmost island in the Pacific, 1200 km south of Okinawa, to ACH by boat. These colonies spawned in the tank in June 2007 and, using the techniques developed by AMSL, numerous coral propagules were produced in a land facility. In April 2008, about 65,000 Acropora colonies were transplanted to the native coral reefs of Okinotorishima (Sato et al. 2010). It is hoped that the corals grow well so that habitat of fish resources will be increased and the tiny Okinotorishima’s landmass will be reinforced by accumulating a thousand tons of coral sand. So far, humans have never tried to accelerate the natural island-building processes. Even if the most advanced civil engineering and coral culture and transplantation techniques are used, it will take some decades before the island becomes large enough to be useful. As a research project, however, it is an exciting challenge to consider the possibility of restoring the coral reefs of small reef islands in the tropics that are sinking underwater due to rising sea levels. As our improved rehabilitation techniques have proved promising, we may be able to overcome the challenges to coral reefs, but only with an understanding that comes with an awakening of the society.

Degradation and restoration of coral reefs in Okinawa Acknowledgements The author appreciates the Nippon Foundation for the financial support for research and education activities at AMSL. He wishes to thank G. Sweany and D.M. Checkley, Jr. for kind reading of the manuscript and helpful discussions. Thanks to two reviewers for their comments and advice on the manuscript.

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