Coral Reef Restoration Handbook - Chapter 16 ppsx

291 16 The Coral Gardening Concept and the Use of Underwater Nurseries: Lessons Learned from Silvics and Silviculture Baruch Rinkevich CONTENTS 16.1 Restoration through the “Coral Reef Gardening” Concept 292 16.2 Corals and Trees — Two Major Framework Building Blocks 293 16.3 Silvics and Silviculture — Still Many Unresolved Issues 293 16.4 Reef Restoration Concepts 294 16.5 A Special Case: Midwater Floating Nursery 295 16.6 Summary 297 Acknowledgment 299 References 299 ABSTRACT The types and numbers of tree species within a forest, as coral colonies in a coral reef, create unique ecosystems by generating biological diversities, formulating the habitats’ three-dimensional structures, and changing local biological and environmental conditions. Resulting from intensive anthropogenic pressure, both ecosystems have lost their resilience, their ability to recover and to self-rehabilitate naturally without active human intervention. However, while forestry practices (silviculture) have been developed and tested worldwide for nearly two centuries, the discipline of active reef restoration is less than a decade old. Nevertheless, even though silviculture actions and concepts have long been subjected to rigorous scientific testing, its applications are still elusive. The situation in the field of reef restoration is even more undefined because the concepts and basic protocols have not yet been well studied. Here, one of the novel tools for coral reef restoration, the “gardening coral reefs” concept, where planned underwater nurseries present forestry principles, is discussed, bearing in mind the lessons learned from silvics and silviculture projects. Furthermore, the recently developed approach of a mid-water floating nursery is explained. In the future, as coral reef restoration may become the dominant conservation approach, there would be the need not only to develop improved protocols and defined conceptual bases, but also to adapt ideas, established expertise, and knowledge from silvicultural experience and science. 2073_C016.fm Page 291 Tuesday, April 18, 2006 11:28 AM © 2006 by Taylor & Francis Group, LLC 292 Coral Reef Restoration Handbook 16.1 RESTORATION THROUGH THE “CORAL REEF GARDENING” CONCEPT The decline of coral reefs worldwide 1–4 has prompted the need for urgent development of adequate restoration methodologies. Restoration itself has also been drawing increasing atten- tion because most efforts to conserve degrading reefs have failed to yield significant results, whereas traditional rehabilitation measures had not successfully compensated for the fast decline. 1,5–7 Moreover, in many reef areas, the poor state of the reef has reached a critical point (sensu 8 ) where management activities could no longer effectively conserve remnants of pre- cious reef populations or prevent further habitat degradation. 7 This situation is further char- acterized by the lack of state-of-the-art remediation protocols, i.e., established theories and approved restoration techniques, specifically developed for the marine environment, including coral reefs. Existing measures still lag behind those developed for terrestrial habitats. 9–11 As a result, the principles underlying remediation measures have turned out to be just some of the many ill-defined issues of reef restoration. 12,13 It is also evident that restoring any type of degraded reef area is a complex biological and ecological procedure. 14,15 Until recently, most studies on coral reef restoration were based on small-scale, short-term experimental protocols, testing only some ecological/biological attributes. During the last decade, however, worldwide coral reef restoration operations have been more frequently employed and tested in various reef localities, and the concept of active restoration has been acknowledged as an important approach for reef rehabilitation. 1,2,5,13,14 One of the most commonly used methodologies for restoration is direct transplantation of coral material (including entire colonies, fragments, nubbins). While the techniques used for removal of coral material and their transportation and reattachment are straightforward and simple, the varying degrees of success that had been reported indicated significant limitations in the direct transplan- tation methodology. This is caused by the stress imposed on the transplanted coral material, the use of insufficient donor colonies and/or too small fragments, and the disturbances inflicted on the donor coral populations. 12,16,17 In other cases, the failure of corals to recover denuded reef areas also reflects postsettlement mortalities. 18 To alleviate these problems, Rinkevich 5 has suggested the strategy of “gardening coral reefs,” a two-step restoration protocol whose central concept is the mariculture of coral recruits (spats, nubbins, coral fragments, and small coral colonies) in nurseries. Firstly, instead of direct transplantation, large in situ or ex situ pools of farmed corals and spats are constructed. In situ nurseries are installed in sheltered zones where the different types of coral recruits are maricultured to sizes suitable for transplantation. This practice also makes use of minute- size coral fragments that would have died in direct transplantation. Secondly, nursery-grown coral colonies are transplanted to degraded reef sites. This approach is associated with theories of silvics and silviculture. 2 Ex situ and in situ coral reef maricultures (the “gardening” concept) are therefore improve- ments over the common but potentially harmful protocols of direct coral transplantation. Ex situ coral mariculture further supports the high survivorship and growth rates of very small coral material (such as settled planulae larvae or delicate nubbins). This concept has already been tested for its applicability in various coral reefs worldwide. Following the suggestion by Rinkevich, 5 several studies tested the applicability, the feasibility, and the detailed developed protocols for holding corals in nurseries under in situ conditions, 19–22 in flowing seawater ex situ systems, 16 or in closed-seawater ex situ facilities (aquaria, holding tanks. 16,23–28 In situ coral nurseries can supply the transplanting operations with corals adapted to natural reef conditions, 1 while ex situ coral nurseries may facilitate the yield of coral planulae, directly increasing genetic variability of transplanted colonies. 5 Both ex situ and in situ approaches can also provide ample material for restoration year-round, thus reducing the collection of coral colonies from the wild. 27–28 2073_C016.fm Page 292 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC The Coral Gardening Concept and the Use of Underwater Nurseries 293 16.2 CORALS AND TREES — TWO MAJOR FRAMEWORK BUILDING BLOCKS Stony corals and trees are the basic framework building blocks of two major biological ecosystems, coral reefs and rainforests. They share a common ecological role by virtue of their biological properties. 29–32 Both building blocks can be propagated by sexual and asexual reproduction (using ramets, nubbins vs. seeds, seedlings, planulae larvae, spat), have direct impact on their ecosystems (trees stabilize soil, enhance litter production, increase soil organic matter, etc.; corals enhance lithification processes, enhance reef rock formation, etc.), and may increase spatial resilience of ecosystems, and have other similarities. 2 By being the primary habitat constructors, these sessile organisms not only bear similarities in their contribution to the ecosystems’ structural arrangements but also follow similar basic architectural rules in their growth and characteristics of pattern formation. 33 Reef corals and rainforest trees also harbor numerous inhabitants and provide the ecosystem with the structural design and strength to resist physical disturbances such as storms. 2 While coral reefs and rainforests exhibit high resilience even to major natural catastrophes, they have been facing dramatic threats from new types of perturbation, as damaging human activities have rapidly increased in scale and intensity. Forest clearing and land conversion to agriculture lead to soil erosion and desertification. Similarly, a major decline in coral coverage due to manmade physical disturbances leads to the collapse of reef communities and the development of algal reefs. 34 Tree logging is recognized as the major destructive agent of forest areas; 35,36 marine-based recre- ational activities play this role in coral reefs. 1,2 Under regimes of chronic human impacts, both ecosystems undergo dramatic changes in structure and composition of species, 5,36 displaying dimin- ishing capacity to show ecological resilience, to absorb disturbances, to reorganize, and to adapt to changes. In the reef ecosystem, this degradation has been augmented during the last two decades by major bleaching events. 4 Can we utilize the lessons learned from silvics and silviculture? 16.3 SILVICS AND SILVICULTURE — STILL MANY UNRESOLVED ISSUES One of the most important disciplines in forestry is silviculture. Silviculture is the agriculture of trees: how to grow them, how to maximize growth and return, and how to manipulate tree species compositions to meet landowners’ objectives. To understand silviculture, one must first understand silvics. Silvics involves understanding how trees grow, reproduce, and respond to environmental changes. Silviculture is the applied restoration concept of rehabilitation of terrestrial habitats where natural self-regeneration of forests is not applicable. The failure of forest systems to self-regenerate has stimulated the development of various restoration measures that have proven to be effective (liter- ature cited in Putz et al., 2001 37 ). These restoration efforts have succeeded in reversing the trend of deterioration and in creating new habitats for biodiversity. 35 Forest restoration research is categorized into three major scientific approaches: genetics, nursery, and site preparation. The term “site preparation” includes not only mechanical cultivation but also the use of herbicides, fertilizers, insecticides, and other treatments that are applied when establishing plantations. 38 Nursery researchers are inclined to outplant nursery treatments, geneti- cists are inclined to outplant progeny tests, and silviculturalists tend to evaluate site preparation methods. Due to these three different routes and the fragmented approaches, even in this well- studied discipline of forestry, trials that comprise all three major categories are scarce; even those that combine two categories are not common. Trials that combine nursery treatments with site preparation treatments are rare. One example is a study by Barber et al. 39 that qualified nursery treatments (fertilization rates) and site preparation treatments (herbicides) under the same experi- mental design. Nursery/genetic trials were evaluated by Land 40 and genotype/silvicultural interac- tion were studies discussed by only a few authors (i.e., reference 41). 2073_C016.fm Page 293 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC 294 Coral Reef Restoration Handbook Although forest restoration has been an important tool for the conservation, preservation, and maintenance of diversity for more than a century, major obstacles in concepts unification still exist. For example, comparing modes of forest protection between regions in Europe is extremely difficult because of wide variation of strategies, procedures, and constraints; the ways forests have been used historically; their present proximity to major urban centers; and even the definition of what constitutes a forest. 42 In this respect, even in silviculture there has yet to be a single, uniform, and universal model and a universally agreed-upon goal for restoration (such as the percentage of forests, which parts should be protected, etc.). It is accepted that the common denominator for a strict forest reserve is not silvicultural management. However, the ideal nonintervention concept of developing appreciable areas of real untouched forests is not realistic for most protected forests. 42 Spatial heterogeneity, enhancing biodiversity of plantations, silviculture systems, structural analy- ses, and scale of heterogeneity are some of the major unsolved issues of proper restoration measures for degraded forests. 43,44 One interesting concept is the “close-to-nature silviculture” concept, 45 which was formulated at the end of the 19th century, when new paradigms emerged under the motto of “returning to nature.” This concept was examined by numerous studies, and much knowledge was gained from practical experience. However, a closer inspection of the experiences drawn from the past century of applications reveals that the progress made toward the two major original goals, the establishment of mixed stands and the promotion of stand irregularity (reviewed in reference 45) has been insufficient. For that reason, the concept of close-to-nature silviculture is open to various interpre- tations, which mainly depend on the emphasis given to the terms “culture” and “nature” and the values associated with them. These and other silvicultural ideas and protocols should be considered when establishing the first ideas and concepts in active reef restoration. 16.4 REEF RESTORATION CONCEPTS Due to biological, structural, and functional analogies between trees and corals, it is natural to suggest that silviculture concepts (well established or even under trial) should assist in establishing the theoretical and practical concepts for coral reef restoration so that a solid restoration framework can be developed. 2 The strategy of coral mariculture through the gardening concept may prove to be the first such sustainable practice for reef restoration, highly comparable to silviculture in its nature. Therefore, the discussion on “gardening the coral reef,” in light of the already dis- cussed/established ideas in silviculture, is of great importance. It should also be kept in mind that the concept of gardening denuded reef areas is a superior strategy to the more traditional and widely used measure of “coral transplantation,” where the need to harvest coral colonies from existing populations represents a major imperfection. We 1,2,5,17 consider coral mariculture to be a major component in reef restoration, a concept that has so far been overlooked. This strategy, when established and tested in various localities world- wide, may shape the conceptual and practical platform for reef restoration activities. Pertaining to transplantation, in comparison to the harmful practice of harvesting corals from donor reef areas, the establishment of coral nurseries eliminates the need for the extraction of valuable coral material. 1,5,13,14,17 As aforementioned, a protected nursery phase provides the transplanted material with an acclimation period ensuring better survivorship and growth to a size suitable for transplan- tation. The transplantation of nursery-grown “propagules” back into their natal reef helps to prevent extinction of genets and species in degrading sites, thus exercising the “rescue effect” 46 on a local scale by preserving genetic heterogeneity. A coral nursery may also serve as a local species pool that supplies reef-managers with coral colonies for sustainable management. 1,2,5,13 Culturing corals in underwater nurseries may also help in structuring the three-dimensional shapes of developing colonies. 14 Colonial structures emerge as iterative processes of successive layers of material. 47 In branching coral colonies, morphology is established through iteration of two structural units: modules of the 2073_C016.fm Page 294 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC The Coral Gardening Concept and the Use of Underwater Nurseries 295 first order (the zooids) and modules of the second order (the branches). Variations in the branching morphologies of colonial organisms are frequently correlated with a suite of life-history traits. 48 A significant part of relevant literature examines correlations between environmental qualities and morphometric analyses (either on the zooid, ramet, or genet level, see references 49–55 and literature therein. While there is no doubt that environmental factors may tune phenotypic architecture (this issue is another factor to be studied in underwater coral nurseries), the common high-fidelity of morphological structures that may be exhibited by any species of coral reveals developmental homeostasis, controlled by the genetic background of the species of interest. 56 Adapted maricultural conditions may therefore “secure” the blueprint structures of developing coral colonies. 14,56 Another interesting genetic approach is the application of “tree architectural models” to coral growth forms, see references 33,57,58 and literature therein. Analyses revealed common rules for branching and ramifying axes systems, for the organization of these axes in identical architectural models, for reiteration patterns in the course of growth, and for the physiological variations correlated with environmental parameters. Much of the literature on ecological restoration pertains to the choice of species to be used. 59 Taxa used for restoration are not selected randomly but often conform to the definition of “key species”; i.e., they perform a function that is more vital for the ecosystem than those of other species. Selected coral species for mariculture are often good representatives of local common coral species and in many cases, are of the branching coral forms. 1,17,19,60 Branching forms are also selected for their high performance in restoration (i.e., survivorship and growth rates). Branching coral colonies potentially provide an increased variety of coral material types that can be used for mariculture including ramets (incorporating a single or several branches); nubbins (fragments the size of a single or several polyps); small whole colonies removed from shallow, frequently disturbed areas, where long-term survival is unlikely; and planula larvae. 1,5,13,61 16.5 A SPECIAL CASE: MIDWATER FLOATING NURSERY Only recently, active coral reef restoration has begun to be viewed as a necessary measure, 61 and it has been accepted that methodology should be appropriately adapted to local socioeconomic limitations and subjected to landscape conditions. The nursery component of the gardening concept, however, is a ubiquitous measure that is likely applicable to all locations and could be installed even away from the reef-site itself. 17 Coral nurseries, like tree plantations, are a stark contrast to constructionally complex, multicohort mature and developed reef areas/forests. However, nurseries, as a rehabilitation tool, facilitate complexity and management of the natural habitats by providing flexibility to meet a range of needs, objectives, and specific aims. 62 Although a wide application of reef restoration requires management approaches that are specifically adapted to different oper- ational situations and local conditions, this discipline still needs a ubiquitous rationale to be developed specifically for coral reef rehabilitation. 5,13 Management decisions should always take into consideration the appropriate target coral species and the type of source material most suitable for local cultivation. As such, site-specific considerations and the use of different local coral species as donors require the development of different specific protocols, tailored to the conditions at dissimilar reef areas. The gardening concept, then, could contribute to the formation of a meaningful reef mitigation framework via the conservation of endangered coral species through mariculture of specific genets and rehabilitation through their transplantation. However, dealing with the specifics without formulating the concepts may be a major obstacle for the development of this scientific discipline. To date, all in situ coral nurseries were studied in constructions at or near sea bottom, in shallow- water reef areas. 1,22 These nurseries were subjected to local conditions and therefore, a ubiquitous rationale has not been developed. A novel general approach for an in situ coral nursery, the establishment of a midwater nursery (14 m above substrate and in 6 m depth; Figure 16.1) in a protected site, 8 km north of major natural reef areas in the Gulf of Eilat, Red Sea has been tested 2073_C016.fm Page 295 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC 296 Coral Reef Restoration Handbook for the first time. 17 This floating nursery, situated away from afflictions of recreational activities and corallivorous organisms, proved to be superior to former versions. More than 7100 coral branches sampled from 11 branching scleractinian species had, after 5 to 10 months, very low (<10%) mortality rates (in some species even zero mortality; Figure 16.2) and very fast growth rates, forming within this limited time frame large colonies originating from small branches (an example case is depicted in Figure 16.3). Since being afloat in midwater (Figure 16.1), this type of nursery demonstrated that: 1. Water flow in this unique nursery system supplies the developing corals with increased quantities of plankton particles, probably with enhanced rates of dissolved oxygen around coral tissues, resulting in more efficient removal of mucus secreted by the coral tissue. 2. Although sea-bottom nurseries are attached to the reef floor, 1,22 and water movement around the corals results strictly from currents or wave actions, in a midwater floating nursery the entire nursery swings in all directions. This flexibility helps to get rid of debris, sediment particles, and other settling material that might accumulate on devel- oping coral colonies. 3. Since in a midwater nursery the substrate is far below, sedimentation is reduced to a minimum with negligible influence on the developing coral colonies. 4. With proper consideration, a midwater nursery can be positioned at different depths, “tailored” for any coral species–specific needs. Using the midwater nursery also allows the developing corals to gradually acclimatize to conditions of depth and radiation similar to those in their designated transplantation site. FIGURE 16.1 A mid-water nursery. A prototype that has recently been tested in the Gulf of Eilat (size 10 × 10 m, made of a rope net; adapted from reference 17). The nursery is connected to the sea bottom (20 m depth) by metal cables and is held floating at 6 m depth by several buoys. Coral colonies are maricultured within plastic nets stretched over PVC frames (30 × 50 cm each). Each frame holds up to 110 pins with coral ramets. The frames were situated in an order that allowed divers to approach the developing coral colonies either from the nursery periphery or from its center. Such a nursery may hold several thousands of coral colonies and can be easily maintained by a single pair of divers. Sea level 0 −6 m −20 m Sea bottom 2073_C016.fm Page 296 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC The Coral Gardening Concept and the Use of Underwater Nurseries 297 5. Installing nurseries at a distance from the coral reef may reduce harmful impacts of corallivorous organisms and recreational activities. 6. Specimens of various commensal and coral-residing species were found to come from the plankton, settling on the newly developed coral colonies ( Trapezia and Tetralia crabs, Spirobranchus giganteus , and others). As a result, transplantation may involve not only the cultured coral colonies but also the entire coral infaunal biodiversity. 17 This floating nursery serves, therefore, as a prototype ubiquitous nursery for developing protocols and working rationales applicable worldwide. 16.6 SUMMARY Ecosystem management in both terrestrial and marine habitats is associated with a blend of social, political, economic, cultural, and ecological themes. 32,63 For example, in silviculture, the choice of methods for thinning forest shading, spacing, and clear-cutting often depend on landowners’ and stakeholders’ demands. As such, selecting which habitat should be restored may be as important as how much is to be restored. Nonrandom restoration practices such as restoring only habitats FIGURE 16.2 Status of ramets from 11 branching scleractinian species ( Millepora, Seriatopora, Stylophora, Pocillopora, and Acropora species) maricultured in the midwater nursery after 5 to 10 nursery months (adapted from reference 17.) FIGURE 16.3 Typical rapid growth of a small Acropora pharaonis branch after 100 nursery days and development into a large colony after 400 nursery days (adapted from reference 17). Scale bar = 1 cm . 0% 20% 40% 60% 80% 100% A. Valida A. Variabilis A. Pharaonis A. Humillis A. Variabilis A. Squarrosa A. Lamarcki Stylophora Pocillopora Millepora Seriatopora Total Coral species Died Detached Lived 2073_C016.fm Page 297 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC 298 Coral Reef Restoration Handbook adjacent to those inhabited by the target species can dramatically reduce or counteract any resto- ration act. 64 Moreover, in many cases of forest management, silvicultural practices are designed to promote the regeneration and the stocking of commercial species for timber forest products, 37 as silviculture involves managing and handling the forest in view of its silvics. Not so in coral reefs. In economically important reef sites (such as for the tourist industry), the coral mariculture strategy is being used to develop sustainable material for human and nonhuman stakeholders in a way that all components of reef habitats benefit. Silviculture is the art and science of producing and tending a forest; application of forest ecology and economics in treatment of forests; and the theory and practice of controlling forest establish- ment, composition, and growth. Through silviculture, we have healthy growing trees, not only for better wood products but also for the environment. In practice, silviculture consists of the various treatments that could be applied to maintain and enhance utility of trees for any purpose. Through harvesting, cutting, thinning, prescribed burning, and various other methods, the variety and age of tree species within a forest, the density of trees, the arrangement of different layers, and other factors such as lighting and shading can be manipulated. It is important to remember that these management techniques not only affect the present forest but also influence its future characteristics. In coral reefs, however, this rationale of active restoration is not yet well accepted. It is probably best exercised in the gardening concept of reef restoration and in restoration of ship grounding sites. Impacts of ship grounding include dislodging and fracturing of corals, pulverizing of coral skeletons, displacement of sediments from ground, and destruction of the three-dimensional struc- tural complexity of the reef. 65 Salvage operations usually add to reef damages, and damages from fuel and cargo slicking from the ruptured hull may worsen the situation. This causes acute and long-lasting effects on regenerative processes of coral communities. Efforts to restore reef sites damaged by ship grounding include such activities as salvaging coral colonies, coral fragments, and sponges; removing loose debris from the reef floor; reconstructing the three-dimensional structural complexity of the reef; and reattaching detached corals and sponges to cleared reef substrates or specially designed artificial reef structures. 65,66 However, a major snag in this type of reef restoration is that most if not all coral material for restoration comes from the damaged sites and not from adjacent coral reef populations. Another challenge to tackle is the massive amount of rubble. The task of emulating natural phenomena of reef growth and development with restoration (as with silviculture to forests 62 ) is challenging, especially when we consider the socioeconomic constraints and our meager knowledge. At present, even the indicators of ecological sustainability of coral reefs are not well defined; there is still no effort to incorporate biodiversity goals into restoration measures, and operational constraints are not designated. Coral reef biologists may adopt 67 the suggestion that any proposed silviculture system designed to maintain biodiversity and produce timber should be treated as a hypothesis due to the limited number of empirical studies to support or refute the approach. Like silviculture, reef restoration deals with the three-dimensional structural topography, the creation of structural topography, and increased heterogeneity. So far, the only active reef restoration principle suggested (and applied) with an eye to ecological principles tested in other similar ecosystems is the gardening concept. 1,2,5,13,14,17 In the coral reef as in forest ecosystems, a “total protection” approach would secure and preserve only a certain number of habitats of rare species in any locality. Therefore, silvicultural management or reef restoration is essentially required to maintain large-scale biodiversity in multifunctional production forests and coral reefs. 5,13,42 The restoration of coral reefs, therefore, should become a standard part of conservation practices, and when applied, already tested and approved forest restoration principles may provide important insight into the understanding of the reef ecosystem recovery. 2 The ability to produce and develop many new coral colonies in nurseries 17 may change the way end-users will manage denuded reef areas in the future. 2073_C016.fm Page 298 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC The Coral Gardening Concept and the Use of Underwater Nurseries 299 ACKNOWLEDGMENT This study was supported by BARD (US-Israel Bi-national Agricultural Research and Development Fund), by an INCO-DEV project (REEFRES), by a World Bank/GEF project (Reef Remedia- tion/Restoration Working Group), and by the AID-CDR program (no. C23-004). REFERENCES 1. Epstein, N., Bak, R.P.M., and Rinkevich, B., Strategies for gardening denuded coral reef areas: the applicability of using different types of coral material for reef restoration, Restor. Ecol., 9, 432, 2001. 2. Epstein, N., Bak, R.P.M., and Rinkevich, B., Applying forest restoration principles to coral reef rehabilitation, Aquat. Conserv ., 13, 387, 2003. 3. Wilkinson, C.R., Status of Coral Reefs of the World: 2002 . Australian Institute of Marine Science, Townsville, Queensland 378 pp, 2002. 4. Bellwood, D.R., Hughes, T.P., Folke, C., and Nyström, M., Confronting the coral reef crisis, Nature , 429, 827, 2004. 5. Rinkevich, B., Restoration strategies for coral reefs damaged by recreational activities: the use of sexual and asexual recruits, Restor. Ecol. 3, 241, 1995. 6. Risk, M.G., Paradise lost: how marine science failed the world’s coral reefs, Mar. Freshwater Res., 50, 831, 1999. 7. Epstein, N., Bak, R.P.M., and Rinkevich, B., Alleviating impacts of anthropogenic activities by traditional conservation measures: can a small reef reserve be sustainedly managed? Biol. Conserv., 121, 243, 2005. 8. Young, T.P., Restoration ecology and conservation biology, Biol. Conserv., 92, 73, 2000. 9. Allison, G.W., Lubchenko, J., and Carr, M.H., Marine reserves are necessary but not sufficient for marine conservation, Ecol. Appl., 8, 79, 1998. 10. Keough, M.J., and Quinn, G.P., Legislative vs. practical protection of an intertidal shoreline in South eastern Australia, Ecol. Appl., 10, 871, 2000. 11. Rose, K.A., Why are quantitative relationships between environmental quality and fish populations so illusive? Ecol. Appl., 10, 367, 2000. 12. Edwards, A.J., and Clark, S., Coral transplantation: a useful management tool or misguided meddling? Mar. Poll. Bull ., 37, 8, 1998. 13. Rinkevich, B., Steps towards the evaluation of coral reef restoration by using small branch fragments, Mar. Biol., 136, 807, 2000. 14. Epstein, N., and Rinkevich, B., From isolated ramets to coral colonies: the significance of colony pattern formation in reef restoration practices, Basic Appl. Ecol., 2, 219, 2001. 15. Omori, M., and Fujiwara, S. (Eds.), Manual for restoration and remediation of coral reefs, Nature Conservation Bureau, Ministry of Environment, Japan, 2004. 16. Becker, L.C., and Mueller, E., The culture, transplantation and storage of Montastraea faveolata, Acropora cervicornis, and Acropora palmata: what we have learned so far, Bull. Mar. Sci., 69, 881, 2001. 17. Shafir, S., van Rijn, J., and Rinkevich, B., A mid water coral nursery, Proc. 10th Int. Coral Reef Symp., in press. 18. Fox, H.E., Coral recruitment in blasted and unblasted sites in Indonesia: assessing rehabilitation potential, Mar. Ecol. Prog. Ser., 269, 131, 2004. 19. Bowden-Kerby, A., Coral transplantation in sheltered habitats using unattached fragments and cultured colonies, 8th Int. Coral Reef Symp., Panama, 2, 63, 1997. 20. Oren, U., and Benayahu, Y., Transplantation of juvenile corals: a new approach for enhancing colo- nization of artificial reefs, Mar. Biol., 127, 499, 1997. 21. Epstein, N. Bak, R.P.M., and Rinkevich, B., Implementation of small scale “no-use zone” policy in a reef ecosystem: Eilat’s reef-lagoon 6 years later, Coral Reefs 18, 327, 1999. 22. Soong, K., and Chen, T., Coral transplantation: regeneration and growth of Acropora fragments in a nursery, Restor. Ecol., 11, 62, 2003. 2073_C016.fm Page 299 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC 300 Coral Reef Restoration Handbook 23. Richmond, R. Coral reef health: concerns, approaches and needs. Proc. Coral Reef Symp. Practices, Reliable, Low Cost Monitoring Methods for Assessing the Biota and Habitat Conditions of Coral Reefs, Silver Spring, MD, 22, 1995. 24. Carlson, B.A., Organism response to change: what aquaria tell us about nature, Am. Zool., 39, 44, 1999. 25. Raymundo, L.J., Maypa, A.P., and Luchavez, M.M., Coral seeding as a technology for recovering degraded coral reefs in the Philippines, Phuket Mar. Biol. Cent. Spec. Publ. 20, 81, 1999. 26. Szmant, A.M., Coral restoration and water quality monitoring with cultured larvae of Montastraea “annularis” and Acropora palmata. Int. Conf. Sci. Aspects of Coral Reef Assessment, Monitoring and Restoration, Florida, 188, 1999. 27. Borneman, E.H., and Lowrie, J., Advances in captive husbandry and propagation: an easily utilized reef replenishment means from the private sector? Bull. Mar. Sci., 69, 897, 2001. 28. Petersen, D., and Tollrian, R., Methods to enhance sexual recruitment for restoration of damaged reefs, Bull. Mar. Sci., 69, 989, 2001. 29. Yonge, C.M., The nature of reef-building (Hermatypic) corals, Bull. Mar. Sci., 23, 2, 1973. 30. Connell, J.H., Diversity in tropical rain forests and coral reefs, Science, 199, 1302, 1978. 31. Goreau, T.F., Goreau, N.I., and Goreau, T.J., Corals and coral reefs, Sci. Am., 241, 110, 1979. 32. Christensen, N.L., Bartuska, A.M., Brown, J.H., Carpenter, S., D’Antonio, C., Francis, R., Franklin, J.F., MacMahon, J.A., Noss, R.F., Parsons, D.J., Peterson, C.H., Turner, M.G., and Woodmansee, R.G., The report of the Ecological Society of America committee on the scientific basis of ecosystem management, Ecol. Appl., 6, 665, 1996. 33. Dauget, J M., Application of tree architecture models to reef-coral growth forms, Mar. Biol., 111, 157, 1991. 34. Lugo, E.L., Caroline, S.R., and Scott, W.N., Hurricanes, coral reefs and rainforests: resistance, ruin, and recovery in the Caribbean, Ambio, 29, 106, 2000. 35. Dobson, A.P., Bradshaw, A.D., and Baker, A.J.M., Hopes for the future: restoration ecology and conservation biology, Science, 227, 515, 1997. 36. Noble, I.R., and Dirzo, R., Forests as human-dominated ecosystems, Science 277, 522, 1977. 37. Putz, F.E., Blate, G.M., Redford, K.H., Fimbel, R., and Robinson, J., Tropical forest management and conservation of biodiversity: an overview, Conserv. Biol., 15, 7, 2001. 38. South, D.B., Rose, R.W., and McNabb, K.L., Nursery and site preparation interaction research in the United States, New Forests, 22, 43, 2001. 39. Barber, B.L. Messina, J.S., van Buijtenen, J.P., and Wall, M.M., Influence of nursery fertilization, site quality, and weed control on first-year performance of outplanted loblolly pine, 6th Biennial Southern Silvicultural Res. Conf., Memphis, TN, 27, 1991. 40. Land, S.B., Performance and G-E interactions of sycamore established from cuttings and seedlings, 2nd Biennial Southern Silvicultural Res. Conf., Atlanta, GA, 431, 1983. 41. McDonald, P.M., Mori, S.R., and Fiddle, G.O., Effects of competition on genetically improved ponderosa pine seedldings, Can. J. For. Res., 29, 940, 1999. 42. Parviainen, J., and Frank, G., Protected forests in Europe approaches — harmonising the definitions for international comparison and forest policy making, J. Environ. Manag., 67, 27, 2003. 43. Kerr, G., The use of silvicultural systems to enhance the biological diversity of plantation forests in Britain, Forestry, 72, 191, 1999. 44. Schutz, J P., Silvicultural tools to develop irregular and diverse forest structures, Forestry, 75, 329, 2002. 45. Schutz, J P., Close-to-nature silviculture: is this concept compatible with species diversity? Forestry, 72, 359, 1999. 46. Sinsch, U., Postmetamorphic dispersal and recruitment of first breeders in a Bufo calmamita meta- population, Oecologia, 112, 42, 1997. 47. Kaandorp, J.A., and de Kluijver, M.J., Verification of fractal growth models of the sponge Haliclona oculata (Porifera) with transplantation experiments, Mar. Biol., 113, 133, 1992. 48. Buss, L.W., and Blackstone, N.W., An experimental exploration of Wadington’s epigenetic landstacep, Phil. Trans. R. Soc. Lond., 332, 49, 1991. 49. Chamberlain, J.A. Jr. and Graus, R.R., Water flow and hydromechanical adaptations of branched reef corals, Bull. Mar. Sci., 25, 112, 1975. 2073_C016.fm Page 300 Friday, April 7, 2006 5:15 PM © 2006 by Taylor & Francis Group, LLC [...]... 1996 64 Huxell, G.R., and Hastings, A., Habitat loss, fragmentation, and restoration, Restor Ecol., 7, 309, 1999 65 Jaap, W.C., Coral reef restoration, Ecol Eng., 15, 345, 2000 66 Precht, W.F., Deis, D.R., and Gelber, A.R., Damage assessment protocols and restoration of coral reefs injured by vessel grounding, Proc 9th Int Coral Reef Symp., Indonesia, 2, 963, 2002 67 Simberloff, D., The role of science...2073_C 016. fm Page 301 Friday, April 7, 2006 5:15 PM The Coral Gardening Concept and the Use of Underwater Nurseries 301 50 Bottjer, D.J., Branching morphology of the reef coral Acropora cervicornis in different hydraulic regimes, J Paleontol., 54, 1102, 1980 51 Sebens, K.P., Water flow and coral colony size: interhabitat comparisons of the octocoral Alcyonium siderium, Proc Nat... Restor Ecol., 7, 42, 1999 60 Franklin, H., Christopher, A., Muhando, A., and Lindahl, U., Coral culturing and temporal recruitment in Zanzibar, Tanzania, Ambio, 27, 651, 1998 61 Bowden-Kerby, A., Low-tech coral reef restoration methods after natural transplantation processes, Bull Mar Sci., 69, 915, 2001 62 Palik, B.J., Mitchell, R.J., and Hiers, J.K., Modeling silviculture after natural disturbance... feeding and flow, Proc 8th Int Coral Reef Symp., 2, 1093, 1997 55 Vago, R., Achituv, Y., Vaky, L., Dubinsky, Z., and Kizner, Z., Colony architecture of Millepora dichotoma Forskål, J Exp Mar Biol Ecol., 224, 225, 1998 56 Rinkevich, B., The branching coral Stylophora pistillata: contribution of genetics in shaping colony landscape, Isr J Zool., 48, 71, 2002 57 Dauget, J.-M., La reiteration adaptive,... Paris, 313 (III), 45, 1991 58 Dauget, J.-M., Essai de comparaison entre l’architecture des coraux et celle des vegetaux, Bull Mus Natl His Nat Paris, (4), 16, 39, 1994 59 Lessica, P., and Allendorf, F.W., Ecological genetics and the restoration of plant communities: mix or match? Restor Ecol., 7, 42, 1999 60 Franklin, H., Christopher, A., Muhando, A., and Lindahl, U., Coral culturing and temporal recruitment... 5473, 1984 52 Abelson, A., Galil, B.S., and Loya, Y., Skeletal modification in stony corals caused by indwelling crabs: hydrodynamical advantages for crab feeding, Symbiosis 10: 233, 1991 53 Helmuth, B.S.T., Sebens, K.P., and Daniel, T.L., Morphological variation in coral aggregations: branch spacing and mass flux to coral tissues, J Exp Mar Biol Ecol., 209, 233, 1997 54 Johnson, A., Flow is genet and . science. 2073_C 016. fm Page 291 Tuesday, April 18, 2006 11:28 AM © 2006 by Taylor & Francis Group, LLC 292 Coral Reef Restoration Handbook 16. 1 RESTORATION THROUGH THE CORAL REEF GARDENING”. management or reef restoration is essentially required to maintain large-scale biodiversity in multifunctional production forests and coral reefs. 5,13,42 The restoration of coral reefs, therefore,. (US-Israel Bi-national Agricultural Research and Development Fund), by an INCO-DEV project (REEFRES), by a World Bank/GEF project (Reef Remedia- tion /Restoration Working Group), and by the AID-CDR