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An economic and ecological consideration of commercial coral transplantation to restore the marine ecosystem in Okinawa, Japan
Ecosystem Services 11 (2015) 39–44
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Ecosystem Services journal homepage: www.elsevier.com/locate/ecoser
An economic and ecological consideration of commercial coral transplantation to restore the marine ecosystem in Okinawa, Japan Nami Okubo a, Ayumi Onuma b,n a b
Department of Economics, Tokyo Keizai University, 1-7-34 Minamimachi, Kokubunji, Tokyo 185-8502, Japan Faculty of Economics, Keio University, 2-15-45 Mita, Minato-ku, Tokyo 108-8345, Japan
art ic l e i nf o
a b s t r a c t
Article history: Received 2 February 2014 Received in revised form 29 May 2014 Accepted 26 July 2014 Available online 27 September 2014
The deterioration of coral reefs in Japan is a serious environmental problem. Conventional conservation policies for terrestrial ecosystems are sometimes difficult to apply to coral reef protection because of the large number of stakeholders involved. In what seems to be an interesting attempt to solve this problem, tourist divers in Okinawa, Japan have begun to transplant coral fragments onto deteriorated coral reefs, by participating in a tour provided by diving shops. However, the problem here is that when the transplanted fragments have been taken out from the natural coral colonies, it tends to cause a host of potential problems such as decreasing fecundity of donor colonies, negative effects on the surrounding environment of the exploited corals and low species diversity of transplanted fragments. In this paper, we examine the merits of commercial coral transplantation in marine ecosystem conservation, and to suggest some reforms that could help to mitigate the problems encountered when using sexually propagated coral transplants. Finally, we discuss how the commercial transplantation in Okinawa could be applied to the conservation of other marine ecosystem. & 2014 Elsevier B.V. All rights reserved.
Keywords: Marine ecosystem restoration Coral reefs Coral transplantation Sexually propagated coral transplants
1. Introduction Undoubtedly, the benefits from ecosystem services provided by coral reefs to humans are remarkably high. Despite this, nonetheless, over the past decades, coral reefs throughout the world have degraded at an alarming rate (Cesar et al., 2003; Costanza et al., 1997). Recent assessment based on annually pooled survey data suggests that the estimated annual loss of coral cover was about 1% over the last 20 years and 2% (or 3168 km2 per year) between 1997 and 2003 (Bruno and Selig, 2007). Wilkinson (2008) reported that 19% of the historically extant coral reefs have already been lost, and an additional 15% will soon be lost. Some evidence indicates that this ecosystem may not be able to recover naturally from anthropogenic stress (Rinkevich, 2005). In Japan, the deterioration of coral reefs has been a serious environmental problem. For instance, the reefs surrounding Okinawa in southern Japan were devastated by a bleaching event. Such incident has dramatically reduced the abundance of many susceptible coral species in the region. An analysis of region-scale coral cover and species abundance at 17–20 sites on the turbid
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Corresponding author. Tel.: þ 81 3 5427 1345. E-mail address: [email protected] (A. Onuma).
http://dx.doi.org/10.1016/j.ecoser.2014.07.009 2212-0416/& 2014 Elsevier B.V. All rights reserved.
reefs of Okinawa Island (total of 79 species, 30 genera, and 13 families) from 1995 to 2009 indicates that coral cover surrounding the sites concerned has decreased drastically from 24.4% to 7.5% (1.1% per year) due to bleaching events occurred in 1998 and 2001 (Hongo and Yamano, 2013). Here, it may be remarked that conventional conservation policies for terrestrial ecosystems have not been able to contribute meaningfully in protecting the coral reef from degradation because of a large number of stakeholders involved. These include fishermen, diving shop owners, animal husbandry who shed excess waste to the rivers, and farmers who dispose pesticides and fertilizers into the sea, and land developers who indulged in land reclamation in coastal areas. In addressing these environmental degradation issues, the stakeholders especially the fishermen and divers should refrain from causing damage to the coral reefs when carrying out their social or economic activities. By the same token, the farmers and land developers are required to adopt more sustainable forms of agricultural or land development practices. In view of varied causal factors, which required different remedial measures, it would be difficult if not impossible to have a one-size-fits all solution in addressing each environmentally unfriendly activity, such as setting a tax on carbon emission in the context of climate change. In an attempt to proliferate corals and to restore the reefs, the transplantation of coral heads or artificially produced coral
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transplants (abbreviated as APTs) is now conducted in Okinawa. Such technique of APT is like cutting propagation of trees by using asexual reproduction, and in several countries this technique has also been used to rescue the endangered corals from various disturbances (Rinkevich, 2014) such as ship groundings, harbor construction and shore embankments. The transplantation project was launched between 2012 and 2016 by using 90,000 APTs in 3 ha of coral farm in Onna- and Yomitan villages. According to Okinawa prefecture, the budget for project in its first three years of implementation is roughly 625 million JPY (6.25 million USD). However, despite the increasing number of restoration activities, the discipline of coral transplantation remains in its formative stage. Clark and Edwards (1995) indicated that considerable uncertainty about the effectiveness and efficiency of coral transplantation still exists. For example, the mortality of transplanted fragments is highly site- and species-specific (Edwards and Clark, 1999). For instance, the survival rates at two different locations using tabular coral Acropora hyacinthus were 24% in the first year (Japan Marine Science and Technology Center, 1991), 44% in the 17th month (Plucer-Rosario and Randall, 1987), and 49% in the second year (Clark, 1997). Another study shows that the mortality rate can also be season-specific. For example, the mortality rate of a 5–10 cm sized Acropora fragment, which has the similar size of the commercially transplanted fragment in Okinawa, varied between 0% and 80% for 2 years depending on when the transplantation is conducted. In particular, APTs are prone to typhoon destruction (Okubo et al., 2007). Hence, relying on generalizations to guide transplantation is dangerous (Edwards and Clark, 1999). However, the transplantation has a role to accelerate the recovery of damaged reef and the reason for it appears to be the human impatience with the speed of natural recovery processes (Edwards, 2010). While the transplantation is never a cheap method, the transplantation in Okinawa is commercially implementing restoration, in which tourist divers as well as the firms conducting Corporate Social Responsibility (CSR) shoulder the cost of transplantation. This paper aims to discuss some merits and problems arising from the transplantation in Okinawa, and to derive some lessons that may be applicable to the conservation of coastal ecosystems in other areas of the world. In addition, the paper gives some suggestions that could help to mitigate the ecological problems of commercial coral transplantation as noted above. We argue that in reforming transplantation efforts, it is important to include more sexually propagated coral transplants (abbreviated as SPTs) in a “basket” of corals, which comprised of a controlled and predetermined mixture of APTs and SPTs. We argue further that naturally occurring fragments from typhoons could be used for transplantation purpose.
2. Transplantation and its practice in Okinawa, Japan In Okinawa, coral transplantation has a distinctive feature in that it is conducted under ecotourism, with the name of “Restore the degrading coral reefs”, though it will be realistically impossible to cover all the degraded reefs by only APTs. Under this ecotourism-based transplantation process, a diving tour is developed in which tourist divers provide services to transplant APTs under the sea on a voluntary base, i.e., they are not paid for the transplantation work. Representative sites of the commercial transplantation are near the harbors of Chatan Town and Onna village located in the main island of Okinawa. The fee of the diving tour provided by the operators includes the fee of the APTs, i.e., the cost of the APTs is passed to the divers. A popular tour consists of two dives in a half-day's tour, one for
transplanting and the other for leisure. The cost is 15,750 yen (some 150 US dollars) including insurance and the cost of boat and tank. Although providing labor services for free can be seen in many cases for people to contribute to restoring the environment on a voluntary basis, the Okinawa case is that the contributors also pay for the cost of APTs and yet derive utility from the cost incurred in term of personal enjoyment. Fragments can be taken from natural colonies after being permitted by Okinawa prefecture and the collected fragment must be reared at least for six months when the size of fragment grows to be APTs in 6–8 cm. There are at least two Japanese shops, which produce and sell or transplant APTs. Sales of APTs continue to increase through various means of advertising. In addition to this, the shops also receive requests from companies to transplant APTs as a part of the CSR activities. This trend reflects that the scope of CSR activities of Japanese firms is now extending from the reduction of greenhouse gas emissions to biodiversity conservation. The shops undertake the coral transplantation process for the firms at a price of 3500 yen (35 USD) per APT. The firms concerned can advertise the transplantation as one of their CSR activities. According to an interview conducted with a producer, which started the commercial transplantation in 2005, it has transplanted more than 60,000 pieces of fragments for a number of firms in 9 years since its operation started. However, since the producer did not go further to monitor the progress of the transplanted corals after the transplantation process, we lack of the necessary data to assess whether commercial transplantation has truly contributed to restoring coral reefs in Okinawa, which is one of the major problems of the commercial transplantation as we explain later.
3. Merits in the commercial transplantation in Okinawa Coral reefs give rise to not only huge economic benefit but also ecological advantage to the local economy. In Okinawa, for example, tourism contributed roughly 660 billion JPY (6.6 billion USD) to its economy in 2009, including the ripple effect, according to Okinawa prefecture. No data on the exact economic contribution of coral reef-based tourism in Okinawa exists, but according to the Japanese Ministry of the Environment, the average ratio of coral reef based tourists in Okinawa between 2003 and 2007 was as high as 43.4%. Thus, the loss of these potential tourists is economically damaging.1 Apart from Okinawa, there are more detailed studies of the benefit derived from coral reefs of Great Barrier Reef in Australia, such as Kragt et al. (2009), Polak and Shashar (2013) and Great Barrier Reef Foundation (2009). In particular, Kragt et al. show that, a hypothetical decrease of coral and fish diversity in the Cairns management area of the Great Barrier Reef Marine Park would reduce the number of divers and snorkelers by 80%. Translating this into monetary term, it came to roughly 103 million AUD per year. At the same time, the Oxford Economics (2009) has also demonstrated that the 1 The Ministry of the Environment of Japan (MOEJ) also showed that the travel and recreation cost incurred by the tourists in Okinawa is roughly 232 billion JPY (2.32 billion USD) annually. Indeed, MOEJ has revealed that the economic value of coral reef-recreation and tourism amounts to about 240 billion JPY (2.4 billion USD) annually. However, based on the information (in Japanese) as published in the website of MOEJ (see http://www.env.go.jp/nature/biodic/coralreefs/project/devel opment.html), it may be remarked that the technique employed in ascertaining the value of the coral-reef recreational and tourism appears to be a non-standard one. For instance, although it is stated that the travel cost method (TCM) is used for estimating the value for tourism and recreation, there is a misunderstanding about TCM that the expenditure incurred by the tourists for traveling and the recreational activities is equivalent to the value. Thus the estimated value is far from reflecting a consumer surplus, which normally used to show the value of ecosystem in the context of tourism, and which TCM aims to derive.
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bleaching cost in the region concerned is equivalent to 3.5% of annual GDP. Thus, restoring coral reefs will not only give rise to benefits from the ecological aspect, but also from the local economic perspective. If the restoration is implemented by commercial transplantation as in the case of Okinawa, there are at least three merits in terms of cost savings. First of all, tourist divers and companies conducting CSR shoulder all the cost of transplantation. Let us suppose that the price of transplanting service is 3500 JPY (35 USD). The production cost of the transplant may be computed by deducting the profit margin out of it. According to Ministry of Finance Japan, the average recurring profit margin in Japan is 3– 4%. We adopt 4% here, so the full cost of transplantation practice is roughly 3360 JPY (33.6 USD) per APT. As noted above, all part of the cost is shouldered by the tourist divers themselves. The second merit involves a creation of business opportunity for the local community in Okinawa, which has the highest unemployment rate in Japan. The third merit is that this activity can enlighten those people who are not familiar with the concept of conservation and the importance of restoring the ecological health of the coral reefs. The ecological awareness can be enhanced by attracting these people to the transplanting tour or by impressing the public especially those non-divers with the advertisement of the tour. Raising environmental awareness in this way is more economical than designing a formal or official program of environmental awareness, which is very costly. Summarizing, it may be remarked in the above light that the transplanting APTs in Okinawa can be considered as highly cost effective not only in terms of the transplantation cost incurred but also, in terms of its contribution to the local economy as well as ecological enlightenment among the people in that it does not only reduce the transplanting cost, but also gives benefit to the local economy and enhances the understanding of conservation of the local people.
4. Problems from ecological perspective However, we consider that this commercial transplantation has three potential problems. The first problem is that the fragments used by the diving tours are the ones that are taken from natural coral colonies. The problem here is that the coral reefs in Okinawa are already deteriorated (Hongo and Yamano, 2013). Hence, if additional coral heads are removed, there will be a negative effect on the surrounding environment of the exploited corals (Lewis, 1997). Even if the fragments are taken from natural donor colonies, the number of gametes or growing oocytes will be reduced in both APTs and donor colony (Okubo et al., 2007, 2005, 2009; Szmant-Froelich, 1985). The second problem is that the transplants rarely have species or genetic diversity. The species selected for transplantation are mostly Acropora. As this type of coral looks attractive, and can grow comparatively faster, it can be sold quickly after it becomes a APT in a short time. Most APTs have been produced by the limited number of colonies permitted by Okinawa Prefecture, and the only one or a few colonies that are broken into many small pieces, resulting in no or low genetic diversity of APTs. Accordingly, it may be a concern if these transplants grow, proliferate locally and spawn, the percentage of fertilization in the transplantation site could be low because most of gametes are to be produced by the APTs from the same donor colonies, i.e., the reefs formed using APTs could not connect to the future generations. Another problem is that low genetic diversity could cause mass fatalities caused by bleaching or diseases (Okubo et al., 2010). The third problem is also concerned with the use of transplants that are exploited from nature for cultivation. Even if the activity
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of transplantation was further accepted by the society as a means to restore the coral reefs and given that the size of the market increased, the supply of APTs would be limited. Hence, it is not be possible to satisfy all the demand for the APTs at the prevailing price because exploiting coral fragments from nature is strictly prohibited by Okinawa prefecture in principle. However, extraction may be permitted in exceptional case and under a strict ecological limit imposed by the authority concerned following the application to the prefecture by the producers of APTs. Under this circumstance, the price of the APT would rise due to the growing scarcity. This tends to boost poaching and thus leading further deterioration of natural corals. In an effort to reduce these problems associated with APTs to rebuild coral reefs, we suggest to use the sexually propagated transplants (SPTs) produced from coral embryos. In Japan, the gametes are often found on shores or condensed along the seawall in the morning after mass coral spawning. This is because the fringing reef is close to the land. There is no doubt that these embryos, which are inseminated from gametes directly collected from the wild colonies of various species at the time of spawning, are genetically diverse (Omori and Iwao, 2014). Japanese aquaria and laboratories have tried sexually propagated corals for a long time and succeeded (Funao, 2006; Hayashi and Iwase, 2010; Marine Science Museum, Tokai University, 2007; Misaki, 2003, 2008; Moritaki et al., 2006; Shimonoseki Marine Science Museum, 2008; Noboribetsu-Marine-Park-Nixe, 2007). The Akajima Marine Science Laboratory successfully created a mass culture of SPTs from embryos in 2005, and these Acropora finally reproduced in 2009 (Iwao et al., 2010) (i.e. the full culture was achieved in Acropora corals on a large scale) (Omori, 2005; Omori et al., 2008). If the SPTs were used for the commercial coral transplantation, there would be no damage to nature as most of the gametes and embryos are mortal in the ocean and the natural corals would be left intact from the exploitation. In addition, genetic diversity is inevitably higher in SPTs produced by sexual reproduction than in SPTs. Thus, SPTs are far more desirable compared to APTs from the ecological perspective.
5. Sexually propagated coral transplants and the production cost The disadvantage in the use of SPTs is that the production cost would be much higher than by using APTs as it takes longer time to rear SPT from an embryo to the same size as a APTs. The cost may vary depending on where and how the SPTs are produced and there exists some studies to demonstrate the cost. According to Edwards (2010), the cost of the transplantation can be broken down into 5 items as follows: (i) (ii) (iii) (iv)
collection of source material; setting up coral culture/nursery/hatchery facilities; establishing collected coral material in culture/nurseries; maintenance of corals in culture, transfer of corals from culture/nursery/farm or source reef and attachment at the rehabilitation site; and (v) maintenance and monitoring of transplants at the rehabilitation site.
It may be remarked further in the above light that Guest et al. (2014) estimate the cost of transplantation in the Philippines by using sexually propagated corals. The cost of rearing a coral at an in situ nursery ranges from 19 to 25 USD per transplant, depending on the amount of rearing time, which ranges from 7 to 19
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months.2 When the cost of outplanting a juvenile is added up, which is 4 USD in each case, the total transplanting cost will range from 24 to 29 USD per transplant (see Table 2 in Guest et al. (2013)). This is in sharp contrast to the case of an APT as in Edwards (2010). In Edwards, the most costly item is related to the transfer of corals, which accounts for 50% of the total cost, followed by establishing the transplants the cost of which occupies 26%. The total production cost per APT, except the transfer cost, may be around 1.4 USD. The transplantation cost per survived transplant increases when the survival rate declines. In general, if we denote the survival rate with r and the production cost per transplant with x, then the transplantation cost per a transplant will be x/r USD. Guest et al. (2013) also show this aspect. The survival rate of 2.5 year-old SPTs ranged from 8% to 47% for those with from 7 to 19 months in nursery. The total cost per survived SPTs was found to range from 61 to 284 USD. In Okinawa, according to an interview conducted with a coral shop in Okinawa, one unit of SPT would be sold at the price of 8000 JPY (80 USD), which includes profit. On the other hand, according to Omori and Iwao (2014) in which the cost is estimated in a same way as in Guest et al. (2013), the production cost of SPT could be lower to 750 JPY (7.5 USD). In any case, it is far higher than the cost to produce APTs. We may raise a question here. How high is the cost of producing SPT compared to that of APT? Comparing the estimation in Guest et al. (2013) with Edwards (2010), the total production cost per asexually produced transplant as estimated by the former is about 1.4 USD3 while the cost of producing SPT, as estimated by the latter is about 13.6–17.9 times as high as that of an APT. On the other hand, according to the interview conducted with the same shop as above in Okinawa, the one unit of SPT could be sold at the price of 900 JPY (9 USD) to 1800 JPY (18 USD). Though there is no exact estimation of the production cost of a transplant in Okinawa as in Philippines, the use of the above interview might lead to that the production cost of a SPT is 4.4–8.9 times as high as that of an APT. Thus, if all the transplants were composed of only SPTs, the price of the transplant would rise considerably, while, as explained above, SPTs cause no damage to the natural colonies and their genetic diversity is much higher. Despite these ecological merits, higher prices would lead to a reduction in the transplants purchased by tourist divers and the firms conducting CSR, except by those with high environmental awareness. In particular, in case of tourist divers, a slight rise in price could lead to a considerable reduction of the purchase, because participation in the transplanting tour is in general luxurious and unnecessary (i.e., the price elasticity of the demand can be high in terms of economics). A current diving tour with the transplantation costs about 20% more than a similar tour without the transplantation.4 The price difference must considerably expand if the transplants are replaced with SPTs.5 If such a sharp rise of the tour price reduces dramatically the quantity of demand, this would reduce the profit of the business. This seems to be the main reason why the
2 Villanueva et al. (2012) also estimated from another reef in the Philippines that the production cost of one unit of SPT with 6 months in nursery is 4.4 USD. 3 On the other hand, Shafir et al. (2006) show that the cost of production of the APTs collected from wild colonies in Red Sea, Israel, is between 0.5 USD and 1.0 USD per APTs. 4 A diving shop sells the former tour at the fee of 15,000 JPY (150 USD) and the latter 12,600 JPY (126 USD). 5 If we calculate the price of SPT to be 4 times as high as that of APTs, then the fee of the tour would rise by 9600 JPY (96 USD), using the price difference of 2400 JPY between the prices of current diving tour with and without the transplantation. If SPT is used for the transplantation instead of APTs, the price of the tour will rise to 22,200 JPY (222 USD).
business of the transplantation does not want to shift the use of transplants from APTs to SPTs. Moreover, if the demand is largely reduced, a merit of the commercial transplantation will be lost; it leads to possibly a reduction in volunteers for coral restoration. One way to resolve the problem of the economic and ecological trade-off between the two types of coral transplants is that the transplants should only be made available in what we call a “basket” of corals, which is a controlled, predetermined mixture of APTs and SPTs. The ratio of the mixture can be determined based on the difference of cost and ecological aspects, and also on the demand function of tourist divers for the basket (Okubo and Onuma, 2010). Without this regulation, the divers would ignore the environmental aspects of choosing between SPTs and APTs. In this case, they would choose the cheaper alternative, that is, APTs. By the same token, the diving shops also prefer the APTs which cost less compared to SPTs. The other way is to make the buyers, especially firms conducting CSR, distinguish the ecological merits between the two kinds of transplants. Such distinction may serves as an incentive for them to choose SPTs for the restoration of coral reef than APTs because they are CSR appealing. In the context of climate change, such a successful distinction includes an example of Gold Standard (GS) carbon credit for the use for voluntary carbon offsets, which are created by better environmental projects for sustainable development. Although the creation process of GS credit is more costly, it is highly demanded with a price premium.6
6. Lessons from Okinawa's commercial transplantation Is Okinawa's experience applicable to other marine ecosystem restoration in the world? We have three remarks as follows. First of all, encouraging voluntary contributions to the restoration can be developed on a commercial basis; at least if the targeted site is the place frequented by many tourists. Indeed, the commercial transplantation operators in Okinawa have contributed fruitfully to such an effort by re-designing their diving tour in such a way that only one dive is for the transplantation and the other one for leisure as included in the package tour. This will fascinate the tourist divers especially those first timer to experience a voluntary activity of transplanting which is ecologically appealing. At the same time, such activity would help to raise environmental alertness among the sea lovers on the importance to protect the coral reefs. Besides, having the two-dive packages design is also more economically appealing to the divers, because the additional cost is only from one transplantation. This will encourage more divers to participate in the voluntary coral reef restoration program. Nonetheless, one caveat is that if the voluntary work is too timeconsuming and leaves little time for leisure, it might attract only a small number of participants. Secondly, despite expanded efforts being made by the commercial base restoration operators in Okinawa to restore the coral reefs, they have not gone far enough to ensure the long-term protection of their ecological integrity. This is because their restoration efforts, are, to a greater extent, dictated by profit motives rather than ecological protection. The use of APTs rather than SPT in the transplantation reflects this aspect. In light of the above, one may argue that it is desirable for the supply-side of the transplants, namely, the producers and the diving shops, to be fully ecological friendly from the outset. However, meeting all aspects of ecological consideration at the outset might raise operational cost considerably. This may serve as 6
See the Gold Standard web page.
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a barrier to entry or the demise of the business due to the lack of economic incentives. The way forward to mitigate this problem is to introduce ecological considerations in stages. Indeed, it is not too late to make the supply-side reformed after the business gets on track, provided that the restoration is not carried out on a large scale basis. In fact, this has taken place in the commercial transplantation. In the early days of the transplantation, the supply-side rarely monitored the survival rate of APTs after the tour. This is also a likely phenomenon for the private companies. The reason behind this is that monitoring after the transplantation does not produce much impact on the increase in the number of customer. Rather, it only serves to increase the cost of the transplantation. This in turn will raise the price of transplants higher if the shops were to include the costs of monitoring after transplantation.7 Despite this, nonetheless, it seems that some diving shops are now introducing the monitoring process into the transplanting operation although they are yet to move towards using SPT. In light of the forgoing, it may be remarked that the natural restoration of the marine ecosystem on a commercial basis should be approved and promoted only if sufficient ecological requirements are satisfied during a defined period rather than from the outset. The length of the defined period should be determined based on the ability of the supply-side to meet the ecological requirements. An example here is to obligate to use SPTs by a certain ratio of total transplants as noted above. The ratio may be gradually increased within the period. Finally, enhancing the interest of the demand-side for a more ecologically friendly restoration is important. To persuade the demand-side to contribute more to such a restoration is possible even though it is often more expensive due to the restoration cost incurred. Nonetheless an interest party who is ecologically conscious may be willing to shoulder the additional cost. If this takes place, a price premium or a supply-side gain would arise and thus encouraging the firms to move towards using SPT technique even though it is more costly. Supplying transplants based on a mixture combination could help to promote sustainable usage of SPTs and at the same time enlightening consumers on the importance of ecological protection at the time of purchase.
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effectiveness and sustainability of transplantation might be a preferable direction. This may be achieved by reforming the transplantation efforts to include more SPTs. In fact, Iwao et al. (2010) reported that the SPTs spawned for the first time 4 years after being cultured from eggs. It means that the APTs can be exploited from the corals that have grown from SPTs, not from the natural colonies. This will lower the cost of coral transplantation considerably in the long run, and thus enable us to use only SPTs at a lower cost. Apart from SPTs, there are other resources that could be used for the transplantation in Okinawa, which are corals of opportunity (Okubo et al., 2007; Garrison and Ward, 2011; Okubo, 2014). However, the prefecture prohibits the use of them as they cannot be distinguished from the artificially taken fragments, for example, by poaching (Nature Conservation Division, 2008). The naturally occurring fragments rarely survive when they detached from the sea bed (Smith and Hughes, 1999), and thus it would be more sensible to establish a way to use them instead of taking fragments from natural corals, though sustainable supply of APTs might not be easy in this case. Certification systems such as the Forest Stewardship Council (FSC) in timber trade could be effective in this case (UNEP-WCMC, 2011). For example, a governmental organization could periodically collect fragments occurred by typhoons and sell them to the shops with a certification as naturally occurred fragments. There are many examples that show how banning the use of natural resources did not work for conservation including coral reefs (Mora et al., 2006). It is possible that establishing a certification system and encouraging the appropriate use of SPTs could lead to more sustainable coastal marine protection. This paper sheds light on this aspect. The present work may be further extended in future research by taking into consideration of the willingness to pay of divers for a diving tour in which the transplants are not APTs but SPTs. Such a study would contribute to effectively designing a commercial-based transplantation system that could be more sustainable from the ecological as well as economic points of view.
Acknowledgments 7. Discussion Edwards (2010) summarized the scale of degradation versus that of restoration: there is a six orders of magnitude mismatch between the damaged area and the level of restoration that can be achieved. The scale of the damage is now enormously large with a wide range of local human impacts on reefs act at scales of several square kilometers (Edwards and Gomez, 2007). This implies that the restoration by the transplantation cannot catch up with the rate of degradation. Nevertheless, it is true that the transplantation, which is easy for anyone such as a diver to participate, may be reinforced based on the promotion of environmental consciousness. This may contribute to slow down the rate of degradation of the coral reefs if not implemented to restore. At this point, it is not very wise to claim that the transplantation is not cost effective and to call for other measures such as controlling damaging human terrestrial activities, as this could discourage potential contributors from their efforts in conserving the coral reefs and lower social consciousness toward marine protection. Improving the cost 7 In terms of Villanueva et al. (2012), the monitoring raises the total cost about 30%, though they deal with the cost of producing SPTs, not APTs, so the monitoring could increase the rate of the rise much more in case of the APTs because monitoring cost does not vary between the two kinds of transplants.
We are very grateful to very helpful comments from Choy Yee Keong and Makoto Omori. We also would like to thank Alasdair Edwards, Patricia Milloslavich, Helen Yap, Eldon Ball, Takayuki Sonoyama, Takashi Funao, Takeya Moritaki and Hiroshi Misaki for their help. We would also like to acknowledge two anonymous reviewers, whose comments are highly helpful to improve the manuscript.
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Edwards, A.J., Gomez, E.D., 2007. Reef restoration concepts and guidelines: making sensible management choices in the face of uncertainty.. The Coral Reef Targeted Research & Capacity Building for Management Program, St Lucia, Australia, 38. Funao, T., 2006. Reproduction and growth of Acropora tumida in Suruga Bay. J. Jpn. Assoc. Zool. Gard. Aquar. 47, 126. Garrison, V.H., Ward, G., 2011. “Transplantation of Storm-generated Coral Fragments to enhance Caribbean Coral Reefs: A Successful Method but not a Solution”. International Journal of Tropical Biology and Conservation vol. 60, 59–70. Guest, J., Baria, M., Gomez, E., Heyward, A., Edwards, A., 2014. Closing the circle: is it feasible to rehabilitate reefs with sexually propagated corals? Coral Reefs 33, 45–55. Kragt, M.E., Roebeling, P.C., Ruijs, A., 2009. Effects of Great Barrier Reef degradation on recreational reef-trip demand: a contingent behaviour approach. Australian Journal of Agricultural and Resource Economics. 53, 213–229. Hayashi, T., Iwase, F., 2010. Growth and maturation of the artificially bred Acropora hyacinthus in Shikoku, Japan. Kuroshio Biosph. 6, 14–25. Hongo, C., Yamano, H., 2013. Species-specific responses of corals to bleaching events on anthropogenically turbid reefs on Okinawa Island, Japan, over a 15year Period (1995–2009). PloS One 8, e60952. Japan Marine Science and Technology Center, 1991. Report of the Coral Reef Project, vol. 1, pp. 1–25 (in Japanese). Iwao, K., Omori, M., Taniguchi, H., Tamura, M., 2010. Transplanted Acropora tenuis (Dana) spawned first in their life 4 years after culture from eggs. Galaxea: J. Coral Reef Stud. 12, 47. Lewis, A.R., 1997. Effects of experimental coral disturbance on the structure of fish communities on large patch reefs. Mar. Ecol. Prog. Ser. 161, 37–50. Marine Science Museum, Tokai University, 2007. Favia speciosa. Journal of Japanese Association of Zoos and Aquariums 48, 72. Misaki, H., 2003. Breeding of the Scleractinian corals in the aquarium. J. Jpn. Assoc. Zool. Gard. Aquar. 44, 114. Misaki, H., 2008. Growth and breeding of the Scleractinian coral, Acropora japonica, in the aquarium. J. Jpn. Assoc. Zool. Gard. Aquar. 49, 29–36. Mora, C., Andrèfouët, S., Costello, M.J., Kranenburg, C., Rollo, A., Veron, J., Gaston, K. J., Myers, R.A., 2006. Coral reefs and the global network of marine protected areas. Science 312, 1750–1751. Moritaki, T., Takamura, N., Kotsubo, Y., Asano, S., 2006. Breeding and reproduction of the hard coral (Acropora sp.) in Toba Aquarium. J. Jpn. Assoc. Zool. Gard. Aquar. 47, 126. Nature Conservation Division, Department of Environmental and Community Affairs, Okinawa Prefectural Government. 2008, Okinawa Coral Transplantation Manual. Okinawa Prefectural Government. Noboribetsu-Marine-Park-Nixe, 2007. Rhizotrochus typus. Journal of Japanese Association of Zoological Gardens and Aquariums 48, 72. Okubo, N., 2014. Current situation of coral transplantation in Japan. Rev. Environ. Econ. Policy Stud. 7, 54–57 (in Japanese). Okubo, N., Motokawa, T., Omori, M., 2007. When fragmented coral spawn? Effect of size and timing on survivorship and fecundity of fragmentation in Acropora formosa. Mar. Biol. 151, 353–363.
Okubo, N., Yamamoto, H.H., Nakaya, F., Okaji, K., 2010. Reproduction in cultured versus wild Acropora intermedia colonies: fertilization, larval oxygen consumption and survival. Biol. Bull. 218, 230–236. Okubo, N., Onuma, A., 2010. A mixture of fragments and seedlings is environmentally optimal for coral transplantation. J. Jpn. Coral Reef Soc. 12, 69–80. Okubo, N., Taniguchi, H., Motokawa, T., 2005. Successful methods for transplanting fragments of Acropora formosa and Acropora hyacinthus. Coral Reefs 24, 333–342. Okubo, N., Taniguchi, H., Omori, M., 2009. Sexual reproduction in transplanted coral fragments of Acropora nasuta. Zool. Sci. 48, 442–447. Omori, M., 2005. Success of mass culture of Acropora corals from egg to colony in open water. Coral Reefs 24, 563. Omori, M., Iwao, K., 2014. Methods of Farming Sexually Propagated Corals and Outplanting for Coral Reef Rehabilitation; With List of References for Coral Reef Rehabilitation Through Active. Akajima Marine Science Laboratory, Okinawa, Japan, pp. 1–63. Omori, M., Iwao, K., Tamura, M., 2008. Growth of transplanted Acropora tenuis 2 years after egg culture. Coral Reefs 27, 165. Oxford Economics, 2009. Valuing the effects of Great Barrier Reef Bleaching. Great Barrier Reef Foundation, Australia 2009. Polak, O., Shashar, N., 2013. Economic value of biological attributes of artificial coral reefs. ICES Journal of Marine Science, 904–912. Plucer-Rosario, G.P., Randall, R.H., 1987. Preservation of rare coral species by transplantation: an examination of their recruitment and growth. Bull. Mar. Sci. 41, 585–593. Rinkevich, B., 2005. Conservation of coral reefs through active restoration measures: recent approaches and last decade progress. Environ. Sci. Technol. 39, 4333–4342. Rinkevich, B., 2014. Revuilding coral reefs: does active reef restoration lead to sustainable reefs? Curr. Opin. Environ. Sustain. 7, 28–36. Shafir, S., Van Rijn, J., Rinkevich, B., 2006. Steps in the construction of underwater coral nursery, an essential component in reef restoration acts. Mar. Biol. 149, 679–687. Shimonoseki Marine Science Museum, 2008. Acropora solitaryensis. Journal of Japanese Association of Zoological Gardens and Aquariums 49, 68. Smith, L., Hughes, T., 1999. An experimental assessment of survival, re-attachment and fecundity of coral fragments. J. Exp. Mar. Biol. Ecol. 235, 147–164. Szmant-Froelich, A., 1985. The effect of colony size on the reproductive ability of the Caribbean coral Monastrea annularis (Ellis and Solander). In: Proceedings of the Fifth International Coral Reef Congress, Tahiti, vol. 4, pp. 295–300. UNEP-WCMC, 2011. Review of the Biodiversity Requirements of Standards and Certification Schemes: A Snapshot of Current Practices, CBD Technical Series 63. Secretariat of the Convention on Biological Diversity, Montreal, Canada. Villanueva, R.D., Baria, M.V.B., dela Cruz, D.W., 2012. Growth and survivorship of juvenile corals outplanted to degraded reef areas in Bolinao–Anda Reef Complex, Philippines. Mar. Biol. Res. 8, 877–884. Wilkinson, C. (Ed.), 2008. Status of Coral Reefs of the World. Global Coral Reef Monitoring Network and Reef and Rainforest Research Center. Townsville, Australia, p. 296.
Contents lists available at ScienceDirect
Ecosystem Services journal homepage: www.elsevier.com/locate/ecoser
An economic and ecological consideration of commercial coral transplantation to restore the marine ecosystem in Okinawa, Japan Nami Okubo a, Ayumi Onuma b,n a b
Department of Economics, Tokyo Keizai University, 1-7-34 Minamimachi, Kokubunji, Tokyo 185-8502, Japan Faculty of Economics, Keio University, 2-15-45 Mita, Minato-ku, Tokyo 108-8345, Japan
art ic l e i nf o
a b s t r a c t
Article history: Received 2 February 2014 Received in revised form 29 May 2014 Accepted 26 July 2014 Available online 27 September 2014
The deterioration of coral reefs in Japan is a serious environmental problem. Conventional conservation policies for terrestrial ecosystems are sometimes difficult to apply to coral reef protection because of the large number of stakeholders involved. In what seems to be an interesting attempt to solve this problem, tourist divers in Okinawa, Japan have begun to transplant coral fragments onto deteriorated coral reefs, by participating in a tour provided by diving shops. However, the problem here is that when the transplanted fragments have been taken out from the natural coral colonies, it tends to cause a host of potential problems such as decreasing fecundity of donor colonies, negative effects on the surrounding environment of the exploited corals and low species diversity of transplanted fragments. In this paper, we examine the merits of commercial coral transplantation in marine ecosystem conservation, and to suggest some reforms that could help to mitigate the problems encountered when using sexually propagated coral transplants. Finally, we discuss how the commercial transplantation in Okinawa could be applied to the conservation of other marine ecosystem. & 2014 Elsevier B.V. All rights reserved.
Keywords: Marine ecosystem restoration Coral reefs Coral transplantation Sexually propagated coral transplants
1. Introduction Undoubtedly, the benefits from ecosystem services provided by coral reefs to humans are remarkably high. Despite this, nonetheless, over the past decades, coral reefs throughout the world have degraded at an alarming rate (Cesar et al., 2003; Costanza et al., 1997). Recent assessment based on annually pooled survey data suggests that the estimated annual loss of coral cover was about 1% over the last 20 years and 2% (or 3168 km2 per year) between 1997 and 2003 (Bruno and Selig, 2007). Wilkinson (2008) reported that 19% of the historically extant coral reefs have already been lost, and an additional 15% will soon be lost. Some evidence indicates that this ecosystem may not be able to recover naturally from anthropogenic stress (Rinkevich, 2005). In Japan, the deterioration of coral reefs has been a serious environmental problem. For instance, the reefs surrounding Okinawa in southern Japan were devastated by a bleaching event. Such incident has dramatically reduced the abundance of many susceptible coral species in the region. An analysis of region-scale coral cover and species abundance at 17–20 sites on the turbid
n
Corresponding author. Tel.: þ 81 3 5427 1345. E-mail address: [email protected] (A. Onuma).
http://dx.doi.org/10.1016/j.ecoser.2014.07.009 2212-0416/& 2014 Elsevier B.V. All rights reserved.
reefs of Okinawa Island (total of 79 species, 30 genera, and 13 families) from 1995 to 2009 indicates that coral cover surrounding the sites concerned has decreased drastically from 24.4% to 7.5% (1.1% per year) due to bleaching events occurred in 1998 and 2001 (Hongo and Yamano, 2013). Here, it may be remarked that conventional conservation policies for terrestrial ecosystems have not been able to contribute meaningfully in protecting the coral reef from degradation because of a large number of stakeholders involved. These include fishermen, diving shop owners, animal husbandry who shed excess waste to the rivers, and farmers who dispose pesticides and fertilizers into the sea, and land developers who indulged in land reclamation in coastal areas. In addressing these environmental degradation issues, the stakeholders especially the fishermen and divers should refrain from causing damage to the coral reefs when carrying out their social or economic activities. By the same token, the farmers and land developers are required to adopt more sustainable forms of agricultural or land development practices. In view of varied causal factors, which required different remedial measures, it would be difficult if not impossible to have a one-size-fits all solution in addressing each environmentally unfriendly activity, such as setting a tax on carbon emission in the context of climate change. In an attempt to proliferate corals and to restore the reefs, the transplantation of coral heads or artificially produced coral
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transplants (abbreviated as APTs) is now conducted in Okinawa. Such technique of APT is like cutting propagation of trees by using asexual reproduction, and in several countries this technique has also been used to rescue the endangered corals from various disturbances (Rinkevich, 2014) such as ship groundings, harbor construction and shore embankments. The transplantation project was launched between 2012 and 2016 by using 90,000 APTs in 3 ha of coral farm in Onna- and Yomitan villages. According to Okinawa prefecture, the budget for project in its first three years of implementation is roughly 625 million JPY (6.25 million USD). However, despite the increasing number of restoration activities, the discipline of coral transplantation remains in its formative stage. Clark and Edwards (1995) indicated that considerable uncertainty about the effectiveness and efficiency of coral transplantation still exists. For example, the mortality of transplanted fragments is highly site- and species-specific (Edwards and Clark, 1999). For instance, the survival rates at two different locations using tabular coral Acropora hyacinthus were 24% in the first year (Japan Marine Science and Technology Center, 1991), 44% in the 17th month (Plucer-Rosario and Randall, 1987), and 49% in the second year (Clark, 1997). Another study shows that the mortality rate can also be season-specific. For example, the mortality rate of a 5–10 cm sized Acropora fragment, which has the similar size of the commercially transplanted fragment in Okinawa, varied between 0% and 80% for 2 years depending on when the transplantation is conducted. In particular, APTs are prone to typhoon destruction (Okubo et al., 2007). Hence, relying on generalizations to guide transplantation is dangerous (Edwards and Clark, 1999). However, the transplantation has a role to accelerate the recovery of damaged reef and the reason for it appears to be the human impatience with the speed of natural recovery processes (Edwards, 2010). While the transplantation is never a cheap method, the transplantation in Okinawa is commercially implementing restoration, in which tourist divers as well as the firms conducting Corporate Social Responsibility (CSR) shoulder the cost of transplantation. This paper aims to discuss some merits and problems arising from the transplantation in Okinawa, and to derive some lessons that may be applicable to the conservation of coastal ecosystems in other areas of the world. In addition, the paper gives some suggestions that could help to mitigate the ecological problems of commercial coral transplantation as noted above. We argue that in reforming transplantation efforts, it is important to include more sexually propagated coral transplants (abbreviated as SPTs) in a “basket” of corals, which comprised of a controlled and predetermined mixture of APTs and SPTs. We argue further that naturally occurring fragments from typhoons could be used for transplantation purpose.
2. Transplantation and its practice in Okinawa, Japan In Okinawa, coral transplantation has a distinctive feature in that it is conducted under ecotourism, with the name of “Restore the degrading coral reefs”, though it will be realistically impossible to cover all the degraded reefs by only APTs. Under this ecotourism-based transplantation process, a diving tour is developed in which tourist divers provide services to transplant APTs under the sea on a voluntary base, i.e., they are not paid for the transplantation work. Representative sites of the commercial transplantation are near the harbors of Chatan Town and Onna village located in the main island of Okinawa. The fee of the diving tour provided by the operators includes the fee of the APTs, i.e., the cost of the APTs is passed to the divers. A popular tour consists of two dives in a half-day's tour, one for
transplanting and the other for leisure. The cost is 15,750 yen (some 150 US dollars) including insurance and the cost of boat and tank. Although providing labor services for free can be seen in many cases for people to contribute to restoring the environment on a voluntary basis, the Okinawa case is that the contributors also pay for the cost of APTs and yet derive utility from the cost incurred in term of personal enjoyment. Fragments can be taken from natural colonies after being permitted by Okinawa prefecture and the collected fragment must be reared at least for six months when the size of fragment grows to be APTs in 6–8 cm. There are at least two Japanese shops, which produce and sell or transplant APTs. Sales of APTs continue to increase through various means of advertising. In addition to this, the shops also receive requests from companies to transplant APTs as a part of the CSR activities. This trend reflects that the scope of CSR activities of Japanese firms is now extending from the reduction of greenhouse gas emissions to biodiversity conservation. The shops undertake the coral transplantation process for the firms at a price of 3500 yen (35 USD) per APT. The firms concerned can advertise the transplantation as one of their CSR activities. According to an interview conducted with a producer, which started the commercial transplantation in 2005, it has transplanted more than 60,000 pieces of fragments for a number of firms in 9 years since its operation started. However, since the producer did not go further to monitor the progress of the transplanted corals after the transplantation process, we lack of the necessary data to assess whether commercial transplantation has truly contributed to restoring coral reefs in Okinawa, which is one of the major problems of the commercial transplantation as we explain later.
3. Merits in the commercial transplantation in Okinawa Coral reefs give rise to not only huge economic benefit but also ecological advantage to the local economy. In Okinawa, for example, tourism contributed roughly 660 billion JPY (6.6 billion USD) to its economy in 2009, including the ripple effect, according to Okinawa prefecture. No data on the exact economic contribution of coral reef-based tourism in Okinawa exists, but according to the Japanese Ministry of the Environment, the average ratio of coral reef based tourists in Okinawa between 2003 and 2007 was as high as 43.4%. Thus, the loss of these potential tourists is economically damaging.1 Apart from Okinawa, there are more detailed studies of the benefit derived from coral reefs of Great Barrier Reef in Australia, such as Kragt et al. (2009), Polak and Shashar (2013) and Great Barrier Reef Foundation (2009). In particular, Kragt et al. show that, a hypothetical decrease of coral and fish diversity in the Cairns management area of the Great Barrier Reef Marine Park would reduce the number of divers and snorkelers by 80%. Translating this into monetary term, it came to roughly 103 million AUD per year. At the same time, the Oxford Economics (2009) has also demonstrated that the 1 The Ministry of the Environment of Japan (MOEJ) also showed that the travel and recreation cost incurred by the tourists in Okinawa is roughly 232 billion JPY (2.32 billion USD) annually. Indeed, MOEJ has revealed that the economic value of coral reef-recreation and tourism amounts to about 240 billion JPY (2.4 billion USD) annually. However, based on the information (in Japanese) as published in the website of MOEJ (see http://www.env.go.jp/nature/biodic/coralreefs/project/devel opment.html), it may be remarked that the technique employed in ascertaining the value of the coral-reef recreational and tourism appears to be a non-standard one. For instance, although it is stated that the travel cost method (TCM) is used for estimating the value for tourism and recreation, there is a misunderstanding about TCM that the expenditure incurred by the tourists for traveling and the recreational activities is equivalent to the value. Thus the estimated value is far from reflecting a consumer surplus, which normally used to show the value of ecosystem in the context of tourism, and which TCM aims to derive.
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bleaching cost in the region concerned is equivalent to 3.5% of annual GDP. Thus, restoring coral reefs will not only give rise to benefits from the ecological aspect, but also from the local economic perspective. If the restoration is implemented by commercial transplantation as in the case of Okinawa, there are at least three merits in terms of cost savings. First of all, tourist divers and companies conducting CSR shoulder all the cost of transplantation. Let us suppose that the price of transplanting service is 3500 JPY (35 USD). The production cost of the transplant may be computed by deducting the profit margin out of it. According to Ministry of Finance Japan, the average recurring profit margin in Japan is 3– 4%. We adopt 4% here, so the full cost of transplantation practice is roughly 3360 JPY (33.6 USD) per APT. As noted above, all part of the cost is shouldered by the tourist divers themselves. The second merit involves a creation of business opportunity for the local community in Okinawa, which has the highest unemployment rate in Japan. The third merit is that this activity can enlighten those people who are not familiar with the concept of conservation and the importance of restoring the ecological health of the coral reefs. The ecological awareness can be enhanced by attracting these people to the transplanting tour or by impressing the public especially those non-divers with the advertisement of the tour. Raising environmental awareness in this way is more economical than designing a formal or official program of environmental awareness, which is very costly. Summarizing, it may be remarked in the above light that the transplanting APTs in Okinawa can be considered as highly cost effective not only in terms of the transplantation cost incurred but also, in terms of its contribution to the local economy as well as ecological enlightenment among the people in that it does not only reduce the transplanting cost, but also gives benefit to the local economy and enhances the understanding of conservation of the local people.
4. Problems from ecological perspective However, we consider that this commercial transplantation has three potential problems. The first problem is that the fragments used by the diving tours are the ones that are taken from natural coral colonies. The problem here is that the coral reefs in Okinawa are already deteriorated (Hongo and Yamano, 2013). Hence, if additional coral heads are removed, there will be a negative effect on the surrounding environment of the exploited corals (Lewis, 1997). Even if the fragments are taken from natural donor colonies, the number of gametes or growing oocytes will be reduced in both APTs and donor colony (Okubo et al., 2007, 2005, 2009; Szmant-Froelich, 1985). The second problem is that the transplants rarely have species or genetic diversity. The species selected for transplantation are mostly Acropora. As this type of coral looks attractive, and can grow comparatively faster, it can be sold quickly after it becomes a APT in a short time. Most APTs have been produced by the limited number of colonies permitted by Okinawa Prefecture, and the only one or a few colonies that are broken into many small pieces, resulting in no or low genetic diversity of APTs. Accordingly, it may be a concern if these transplants grow, proliferate locally and spawn, the percentage of fertilization in the transplantation site could be low because most of gametes are to be produced by the APTs from the same donor colonies, i.e., the reefs formed using APTs could not connect to the future generations. Another problem is that low genetic diversity could cause mass fatalities caused by bleaching or diseases (Okubo et al., 2010). The third problem is also concerned with the use of transplants that are exploited from nature for cultivation. Even if the activity
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of transplantation was further accepted by the society as a means to restore the coral reefs and given that the size of the market increased, the supply of APTs would be limited. Hence, it is not be possible to satisfy all the demand for the APTs at the prevailing price because exploiting coral fragments from nature is strictly prohibited by Okinawa prefecture in principle. However, extraction may be permitted in exceptional case and under a strict ecological limit imposed by the authority concerned following the application to the prefecture by the producers of APTs. Under this circumstance, the price of the APT would rise due to the growing scarcity. This tends to boost poaching and thus leading further deterioration of natural corals. In an effort to reduce these problems associated with APTs to rebuild coral reefs, we suggest to use the sexually propagated transplants (SPTs) produced from coral embryos. In Japan, the gametes are often found on shores or condensed along the seawall in the morning after mass coral spawning. This is because the fringing reef is close to the land. There is no doubt that these embryos, which are inseminated from gametes directly collected from the wild colonies of various species at the time of spawning, are genetically diverse (Omori and Iwao, 2014). Japanese aquaria and laboratories have tried sexually propagated corals for a long time and succeeded (Funao, 2006; Hayashi and Iwase, 2010; Marine Science Museum, Tokai University, 2007; Misaki, 2003, 2008; Moritaki et al., 2006; Shimonoseki Marine Science Museum, 2008; Noboribetsu-Marine-Park-Nixe, 2007). The Akajima Marine Science Laboratory successfully created a mass culture of SPTs from embryos in 2005, and these Acropora finally reproduced in 2009 (Iwao et al., 2010) (i.e. the full culture was achieved in Acropora corals on a large scale) (Omori, 2005; Omori et al., 2008). If the SPTs were used for the commercial coral transplantation, there would be no damage to nature as most of the gametes and embryos are mortal in the ocean and the natural corals would be left intact from the exploitation. In addition, genetic diversity is inevitably higher in SPTs produced by sexual reproduction than in SPTs. Thus, SPTs are far more desirable compared to APTs from the ecological perspective.
5. Sexually propagated coral transplants and the production cost The disadvantage in the use of SPTs is that the production cost would be much higher than by using APTs as it takes longer time to rear SPT from an embryo to the same size as a APTs. The cost may vary depending on where and how the SPTs are produced and there exists some studies to demonstrate the cost. According to Edwards (2010), the cost of the transplantation can be broken down into 5 items as follows: (i) (ii) (iii) (iv)
collection of source material; setting up coral culture/nursery/hatchery facilities; establishing collected coral material in culture/nurseries; maintenance of corals in culture, transfer of corals from culture/nursery/farm or source reef and attachment at the rehabilitation site; and (v) maintenance and monitoring of transplants at the rehabilitation site.
It may be remarked further in the above light that Guest et al. (2014) estimate the cost of transplantation in the Philippines by using sexually propagated corals. The cost of rearing a coral at an in situ nursery ranges from 19 to 25 USD per transplant, depending on the amount of rearing time, which ranges from 7 to 19
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months.2 When the cost of outplanting a juvenile is added up, which is 4 USD in each case, the total transplanting cost will range from 24 to 29 USD per transplant (see Table 2 in Guest et al. (2013)). This is in sharp contrast to the case of an APT as in Edwards (2010). In Edwards, the most costly item is related to the transfer of corals, which accounts for 50% of the total cost, followed by establishing the transplants the cost of which occupies 26%. The total production cost per APT, except the transfer cost, may be around 1.4 USD. The transplantation cost per survived transplant increases when the survival rate declines. In general, if we denote the survival rate with r and the production cost per transplant with x, then the transplantation cost per a transplant will be x/r USD. Guest et al. (2013) also show this aspect. The survival rate of 2.5 year-old SPTs ranged from 8% to 47% for those with from 7 to 19 months in nursery. The total cost per survived SPTs was found to range from 61 to 284 USD. In Okinawa, according to an interview conducted with a coral shop in Okinawa, one unit of SPT would be sold at the price of 8000 JPY (80 USD), which includes profit. On the other hand, according to Omori and Iwao (2014) in which the cost is estimated in a same way as in Guest et al. (2013), the production cost of SPT could be lower to 750 JPY (7.5 USD). In any case, it is far higher than the cost to produce APTs. We may raise a question here. How high is the cost of producing SPT compared to that of APT? Comparing the estimation in Guest et al. (2013) with Edwards (2010), the total production cost per asexually produced transplant as estimated by the former is about 1.4 USD3 while the cost of producing SPT, as estimated by the latter is about 13.6–17.9 times as high as that of an APT. On the other hand, according to the interview conducted with the same shop as above in Okinawa, the one unit of SPT could be sold at the price of 900 JPY (9 USD) to 1800 JPY (18 USD). Though there is no exact estimation of the production cost of a transplant in Okinawa as in Philippines, the use of the above interview might lead to that the production cost of a SPT is 4.4–8.9 times as high as that of an APT. Thus, if all the transplants were composed of only SPTs, the price of the transplant would rise considerably, while, as explained above, SPTs cause no damage to the natural colonies and their genetic diversity is much higher. Despite these ecological merits, higher prices would lead to a reduction in the transplants purchased by tourist divers and the firms conducting CSR, except by those with high environmental awareness. In particular, in case of tourist divers, a slight rise in price could lead to a considerable reduction of the purchase, because participation in the transplanting tour is in general luxurious and unnecessary (i.e., the price elasticity of the demand can be high in terms of economics). A current diving tour with the transplantation costs about 20% more than a similar tour without the transplantation.4 The price difference must considerably expand if the transplants are replaced with SPTs.5 If such a sharp rise of the tour price reduces dramatically the quantity of demand, this would reduce the profit of the business. This seems to be the main reason why the
2 Villanueva et al. (2012) also estimated from another reef in the Philippines that the production cost of one unit of SPT with 6 months in nursery is 4.4 USD. 3 On the other hand, Shafir et al. (2006) show that the cost of production of the APTs collected from wild colonies in Red Sea, Israel, is between 0.5 USD and 1.0 USD per APTs. 4 A diving shop sells the former tour at the fee of 15,000 JPY (150 USD) and the latter 12,600 JPY (126 USD). 5 If we calculate the price of SPT to be 4 times as high as that of APTs, then the fee of the tour would rise by 9600 JPY (96 USD), using the price difference of 2400 JPY between the prices of current diving tour with and without the transplantation. If SPT is used for the transplantation instead of APTs, the price of the tour will rise to 22,200 JPY (222 USD).
business of the transplantation does not want to shift the use of transplants from APTs to SPTs. Moreover, if the demand is largely reduced, a merit of the commercial transplantation will be lost; it leads to possibly a reduction in volunteers for coral restoration. One way to resolve the problem of the economic and ecological trade-off between the two types of coral transplants is that the transplants should only be made available in what we call a “basket” of corals, which is a controlled, predetermined mixture of APTs and SPTs. The ratio of the mixture can be determined based on the difference of cost and ecological aspects, and also on the demand function of tourist divers for the basket (Okubo and Onuma, 2010). Without this regulation, the divers would ignore the environmental aspects of choosing between SPTs and APTs. In this case, they would choose the cheaper alternative, that is, APTs. By the same token, the diving shops also prefer the APTs which cost less compared to SPTs. The other way is to make the buyers, especially firms conducting CSR, distinguish the ecological merits between the two kinds of transplants. Such distinction may serves as an incentive for them to choose SPTs for the restoration of coral reef than APTs because they are CSR appealing. In the context of climate change, such a successful distinction includes an example of Gold Standard (GS) carbon credit for the use for voluntary carbon offsets, which are created by better environmental projects for sustainable development. Although the creation process of GS credit is more costly, it is highly demanded with a price premium.6
6. Lessons from Okinawa's commercial transplantation Is Okinawa's experience applicable to other marine ecosystem restoration in the world? We have three remarks as follows. First of all, encouraging voluntary contributions to the restoration can be developed on a commercial basis; at least if the targeted site is the place frequented by many tourists. Indeed, the commercial transplantation operators in Okinawa have contributed fruitfully to such an effort by re-designing their diving tour in such a way that only one dive is for the transplantation and the other one for leisure as included in the package tour. This will fascinate the tourist divers especially those first timer to experience a voluntary activity of transplanting which is ecologically appealing. At the same time, such activity would help to raise environmental alertness among the sea lovers on the importance to protect the coral reefs. Besides, having the two-dive packages design is also more economically appealing to the divers, because the additional cost is only from one transplantation. This will encourage more divers to participate in the voluntary coral reef restoration program. Nonetheless, one caveat is that if the voluntary work is too timeconsuming and leaves little time for leisure, it might attract only a small number of participants. Secondly, despite expanded efforts being made by the commercial base restoration operators in Okinawa to restore the coral reefs, they have not gone far enough to ensure the long-term protection of their ecological integrity. This is because their restoration efforts, are, to a greater extent, dictated by profit motives rather than ecological protection. The use of APTs rather than SPT in the transplantation reflects this aspect. In light of the above, one may argue that it is desirable for the supply-side of the transplants, namely, the producers and the diving shops, to be fully ecological friendly from the outset. However, meeting all aspects of ecological consideration at the outset might raise operational cost considerably. This may serve as 6
See the Gold Standard web page.
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a barrier to entry or the demise of the business due to the lack of economic incentives. The way forward to mitigate this problem is to introduce ecological considerations in stages. Indeed, it is not too late to make the supply-side reformed after the business gets on track, provided that the restoration is not carried out on a large scale basis. In fact, this has taken place in the commercial transplantation. In the early days of the transplantation, the supply-side rarely monitored the survival rate of APTs after the tour. This is also a likely phenomenon for the private companies. The reason behind this is that monitoring after the transplantation does not produce much impact on the increase in the number of customer. Rather, it only serves to increase the cost of the transplantation. This in turn will raise the price of transplants higher if the shops were to include the costs of monitoring after transplantation.7 Despite this, nonetheless, it seems that some diving shops are now introducing the monitoring process into the transplanting operation although they are yet to move towards using SPT. In light of the forgoing, it may be remarked that the natural restoration of the marine ecosystem on a commercial basis should be approved and promoted only if sufficient ecological requirements are satisfied during a defined period rather than from the outset. The length of the defined period should be determined based on the ability of the supply-side to meet the ecological requirements. An example here is to obligate to use SPTs by a certain ratio of total transplants as noted above. The ratio may be gradually increased within the period. Finally, enhancing the interest of the demand-side for a more ecologically friendly restoration is important. To persuade the demand-side to contribute more to such a restoration is possible even though it is often more expensive due to the restoration cost incurred. Nonetheless an interest party who is ecologically conscious may be willing to shoulder the additional cost. If this takes place, a price premium or a supply-side gain would arise and thus encouraging the firms to move towards using SPT technique even though it is more costly. Supplying transplants based on a mixture combination could help to promote sustainable usage of SPTs and at the same time enlightening consumers on the importance of ecological protection at the time of purchase.
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effectiveness and sustainability of transplantation might be a preferable direction. This may be achieved by reforming the transplantation efforts to include more SPTs. In fact, Iwao et al. (2010) reported that the SPTs spawned for the first time 4 years after being cultured from eggs. It means that the APTs can be exploited from the corals that have grown from SPTs, not from the natural colonies. This will lower the cost of coral transplantation considerably in the long run, and thus enable us to use only SPTs at a lower cost. Apart from SPTs, there are other resources that could be used for the transplantation in Okinawa, which are corals of opportunity (Okubo et al., 2007; Garrison and Ward, 2011; Okubo, 2014). However, the prefecture prohibits the use of them as they cannot be distinguished from the artificially taken fragments, for example, by poaching (Nature Conservation Division, 2008). The naturally occurring fragments rarely survive when they detached from the sea bed (Smith and Hughes, 1999), and thus it would be more sensible to establish a way to use them instead of taking fragments from natural corals, though sustainable supply of APTs might not be easy in this case. Certification systems such as the Forest Stewardship Council (FSC) in timber trade could be effective in this case (UNEP-WCMC, 2011). For example, a governmental organization could periodically collect fragments occurred by typhoons and sell them to the shops with a certification as naturally occurred fragments. There are many examples that show how banning the use of natural resources did not work for conservation including coral reefs (Mora et al., 2006). It is possible that establishing a certification system and encouraging the appropriate use of SPTs could lead to more sustainable coastal marine protection. This paper sheds light on this aspect. The present work may be further extended in future research by taking into consideration of the willingness to pay of divers for a diving tour in which the transplants are not APTs but SPTs. Such a study would contribute to effectively designing a commercial-based transplantation system that could be more sustainable from the ecological as well as economic points of view.
Acknowledgments 7. Discussion Edwards (2010) summarized the scale of degradation versus that of restoration: there is a six orders of magnitude mismatch between the damaged area and the level of restoration that can be achieved. The scale of the damage is now enormously large with a wide range of local human impacts on reefs act at scales of several square kilometers (Edwards and Gomez, 2007). This implies that the restoration by the transplantation cannot catch up with the rate of degradation. Nevertheless, it is true that the transplantation, which is easy for anyone such as a diver to participate, may be reinforced based on the promotion of environmental consciousness. This may contribute to slow down the rate of degradation of the coral reefs if not implemented to restore. At this point, it is not very wise to claim that the transplantation is not cost effective and to call for other measures such as controlling damaging human terrestrial activities, as this could discourage potential contributors from their efforts in conserving the coral reefs and lower social consciousness toward marine protection. Improving the cost 7 In terms of Villanueva et al. (2012), the monitoring raises the total cost about 30%, though they deal with the cost of producing SPTs, not APTs, so the monitoring could increase the rate of the rise much more in case of the APTs because monitoring cost does not vary between the two kinds of transplants.
We are very grateful to very helpful comments from Choy Yee Keong and Makoto Omori. We also would like to thank Alasdair Edwards, Patricia Milloslavich, Helen Yap, Eldon Ball, Takayuki Sonoyama, Takashi Funao, Takeya Moritaki and Hiroshi Misaki for their help. We would also like to acknowledge two anonymous reviewers, whose comments are highly helpful to improve the manuscript.
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