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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Opportunities for Biotechnology for Coral and Reef Restoration Aileen N. C. Morse SITUATION AND NEED Coral reef ecosystems are among the most diverse ecosystems on Earth. Their survival and recurrence over geological time indicate that they possess effective mechanisms of acclimation and adaptation to disturbances. Yet, evidence from recent climatic and episodic events indicates the possibility that these mechanisms are being excessively taxed (Buddemeier and Smith 1999; Done 1999). Complex interactions, as yet hardly understood, between effects resulting from the trend in global warming and those from anthropogenic impacts on near-shore reefs are thought to have led to large-scale changes in community structure, bioerosion, tissue mortality, reduced abundance of corals, and increased incidence of disease (Brown and others 1996; Chadwick-Furman 1996; Jokiel and Coles 1990; Smith and Buddemeier 1992). One of the critical consequences of these disturbances has been to reduce effectively the reproductive potential or capacity of many coral communities. Significant numbers of adult reproductive colonies and young recruits have been partially or totally destroyed (Fisk and Done 1985; McField 1999; Meesters and Bak 1993; Wilkinson and others 1999). This situation is a serious threat to the future stability of coral reefs, given that the integrity and diversity of coral reefs is maintained by processes of sexual reproduction and recruitment Marine Biotechnology Center, Marine Science Institute, University of California, Santa Barbara, CA
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP of new corals, vegetative spread of individual colonies, and the reestablishment of colony fragments. Consequently, human intervention as a means to reverse this situation is being considered. Our current understanding of the basic biological and physiological processes and genetics of corals is very limited. It is quite apparent that we simply do not have the technological base to support a concerted effort of reef restoration. If we are to adopt this approach, we must first become better informed about the processes that maintain a healthy reef ecosystem, as well as increase our ability to predict and monitor natural and anthropogenic stresses. These advances will require major technological advances in the areas of coral genetics, coral cultivation, restoration technologies, and molecular physiology. What we do have is a whole range of novel biotechnology approaches recently developed for other areas. Many of these approaches appear to be suitable, after appropriate modification, for direct application to coral reef restoration. Additionally, at present, there is no concerted global funding effort to facilitate rapid sharing of information, on both developing situations that need to be addressed and the development of novel approaches, particularly modern molecular and genetic approaches, to pinpoint emerging problems and solve them. Most of the currently funded research is being conducted at the individual small-group level. We learn of developments after the fact, through publications. For reefs, which are largely distributed in remote, often underdeveloped areas, this is a particular problem that must be addressed. OPPORTUNITIES FOR BIOTECHNOLOGY Genetics The first, most obvious area providing an opportunity for the development and application of a biotechnological approach is that of the genetics of corals. For coral restoration, the first consideration is to be able to produce a source of coral recruits for out-planting into the reef environment and outgrowth in an aquaculture setting for production of young corals for the aquarium trade. In recent years, there has been mass destruction of reefs, particularly in the Pacific, because of indiscriminate acquisition of fish and corals to supply the huge demand of the worldwide aquarium trade. An important consideration when developing a plan for out-planting of new recruits to the reef is the genetic makeup of existing populations of corals, which is still an open question. Recent ecological evidence predicts that most recruitment occurs locally. Sammarco and Andrews (1988) found that the number of recruited larvae significantly decreased with distance from the source of larvae after a
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP mass-spawning event that occurred on the reefs around an island. Hughes and others (1999), in an experiment covering the length of the Great Barrier Reef, found no recruitment to panels in areas of relatively low density of adults; recruitment occurred in areas of the reef where high densities of adults occurred, suggesting that the majority of larvae were locally retained. In contrast, two different lines of evidence suggest that local recruitment comes from distant supplies of larvae. Studies of gene flow incorporating the genetic composition of local and distant populations of adults indicate that the norm is interbreeding among widely distant populations (Ayre 1990; Ayre and others 1997; Bohonak 1999). Additionally, there is ample evidence for the ability of coral larvae to successfully delay metamorphosis (Morse and others 1996; Morse and others 1988; Richmond 1987). Even after several months in the plankton, larvae retain both their stringency of requirement for an external inducer of metamorphosis and specificity of recognition of the required chemical cue. This ability thus confers fitness for long-range dispersal and recruitment to distant reefs. These results imply that molecular genetic information will be required before selecting sources of brood stock for larval recruits. Additionally, genetic screening of all larvae raised in aquaculture facilities will be required to maintain genetic diversity. A recent innovation, gene chip technology (Gerhold and others 1999), should prove to be a very powerful tool in this area. This tool can be modified to address several areas pertinent to reef restoration. DNA/ DNA hybridization could be used for genotyping (DNA mapping and sequencing) to resolve questions of population structure and diversity. DNA/RNA hybridization (gene expression) analyses could identify prevailing environmental parameters or physiological conditions both on the reef and in an aquaculture facility, enabling detection of altered patterns of gene expression as early-warning indicators of stress. Coral Cultivation Restoration of damaged reefs and supply of young corals for the aquarium trade are the two main targets in coral cultivation. The few attempts at stony coral aquaculture (in the Florida Keys) were unsuccessful as viable enterprises. They appear to have failed because of lack of hard scientific data to guide their approach. This situation is very similar to the early history of shellfish aquaculture, particularly that of abalone. The approach was based on anecdotal evidence rather than on scientific fact. Only after funding by the California Sea Grant Program of basic research into the physiology and molecular mechanisms that control reproduction, metamorphosis and grow-out did this industry begin to grow and succeed. There have been prior experimental attempts in Hawaii to
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP reattach coral fragments to small posts, but the lack of success precluded this approach from developing to the commercial stage. Before aquaculture can be considered we will need to develop core technologies for the control of reproduction, larval rearing, metamorphosis, grow-out and out-planting, genetic screening and diversity, and perhaps, in the future, genetic improvement of broodstock. Our purpose will be to produce a multitude of different species in large numbers, under controlled aquaculture conditions. For reef restoration, we will need to produce both complex (branching) and robust (solid) corals; for aquaculture branching, stony corals are the most desirable type. In many invertebrates, the processes of reproduction and larval metamorphosis are regulated by specific environmental molecular signal molecules (Morse 1991; Morse and Morse 1991b). For many years, these processes have been successfully harnessed for control in finfish and shellfish aquaculture; recent investigations have revealed related pathways in corals. Broadcast spawning, fertilization, planktonic behavior and larval settlement, and metamorphosis all depend on molecular recognition of a factor in the environment. Reproduction and spawning in many molluscs is controlled by prostaglandins (Morse 1984). The activity of this hormone can be mimicked by hydrogen peroxide (Morse and others 1977), a simple chemical adaptable for use in aquaculture of many molluscs (Morse and others 1978). We and our colleagues in Japan recently induced Pacific acroporid corals to spawn using both prostaglandins and hydrogen peroxide. The gametes were viable for fertilization; larvae developed normally and metamorphosed in response to the required chemical cue. These results suggest that techniques for inducing spawning in corals in aquaculture could be based on those developed for molluscs. Until very recently, the processes that coordinate synchronous spawning of multiple colonies of numerous stony coral species has been a mystery. Tarrant and others (1999) found that estrogens appear to act as bioregulators of this process, as well as gametogenesis. Development of inexpensive mimics of the identified estrogens, estrone and estradiol-17 beta, will prove useful for control of these processes in an aquaculture setting. The signal molecules that control settlement and metamorphosis in marine invertebrates are not as universal as those controlling reproduction are. These are usually species or group specific. Our understanding of these processes in corals is quite developed. The chemical cue required for metamorphosis is a sulfated polysaccharide of the calcified cell walls of crustose red algae, the algae that cement the reef structure together (Morse and Morse 1991a). Representative corals of four major coral families, Acroporidae, Faviidae, Agariciidae, and Poritidae, all require this same chemical cue (Morse 1998; Morse and others 1996). When examined in the light of recent phylogenetic revisions of corals (Chen and others
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP 1995; Romamo and Palumbi 1996; Veron and others 1996), these data reveal a common ancestry for this mechanism that dates back to 240 Ma (Morse and others 1996). Restoration Technology To restore corals to damaged reefs, it will be necessary to produce coral larvae in an aquaculture setting, raise them to metamorphic competence, induce larvae to metamorphosis on suitable substrates, and out-plant the young recruits onto the reef. To accomplish this objective, we must develop reliable technologies to predict and control gametogenesis, spawning and larval production, induction of larval settlement and metamorphosis, and successful out-planting. There is a critical need to especially address the first and last of these; we already have the beginning of the technological base for controlling metamorphosis. For restoration purposes, we will be relying on the viability of adult corals brought in from the field as brood stock. In the wake of recent bleaching events, it is clear that the reproductive capacity of corals is negatively affected not only by loss of reproductive mass (Fisk and Done 1985; McField 1999) but also by interference with reproductive physiological functions (Glynn 1996; Morse 1996; Rinkevich 1996; Szmant and Glassman 1990). In addition, reproductive capacity is commonly affected by a number of stresses that include hurricanes, typhoons and storms, elevated water temperatures and increased UV irradiance, elevated nutrient and sediment loads, and disease. There is, therefore, a need for the development of new technologies to predict, assess, and analyze reproductive capacity and factors (intervening environmental factors as well as “stressors”) affecting this process. Additionally, we need to update our ability to predict fecundity. To accomplish this, we need to develop simple uniform assays based on the physiological processes involved. Our current methods are unreliable at best. In spite of recent observations of reduced fecundity, the available number of gametes for potential harvest is enormous compared with our ability to harness this resource. Presently, our needs for laboratory-level gamete capture are adequate (Morse and others 1996), but much more efficient technologies must be developed for aquaculture purposes. Identification of the physiological indicators of timing of release of gametes (and assays for their detection) is critical to efficient capture of gametes that are released on only one night of the year. Methods developed for successful fertilization of gametes and rearing of larvae in the laboratory (Morse and others 1996) must be experimentally modified for aquaculture. In this context, we need to identify environmental factors that limit
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP complete gamete development—a bottleneck in fertilization success. There has been recent success in isolating sperm-attractant molecules from a single montiporid species; three highly unsaturated fatty acids in a particular ratio were identified (Coll and others 1994). Results suggest that particular ratios of related fatty acids might act as sperm attractants in a species-specific manner. The finding that corals share a common chemosensory mechanism (Morse and others 1996) has made it possible to develop chemoinductive substrates, or “flypapers,” with proven efficacy in field tests for successful recruitment of larvae on the reef (Morse and Morse 1996; Morse and others 1994). The purified inducer contains both hydrophobic and ionic moieties, and both properties have guided the development and experimentation of different coupling technologies. The most recent of these uses technologies borrowed from the semiconductor industry. A monolayer of the purified inducer is coupled by a linker to a silanized surface, resulting in a highly potent inductive substrate that is active for long periods in seawater. There is still room for further development of this product; we are working on the flexibility of the substrate material. This flypaper technology is ideal for controlled settlement and metamorphosis of larvae for aquaculture. It is anticipated that these substrates will also provide a means of easily out-planting newly settled recruits onto the reef, which we have repeatedly demonstrated in a research situation (Morse 1998; Raimondi and Morse forthcoming). Additionally, they are potentially useful for resolution of other factors involved in recruitment. Examples include monitoring the availability of larvae for recruitment from the plankton; assessing variation in recruitment under different environmental conditions, one indicator of reef health; and offsetting the collection of corals from reefs for the aquarium, jewelry, and ornamental trades and providing an alternative source of coral for medical purposes such as bone replacement. The main criteria that will be used to access the outcome of restoration technology will be establishment of a reproductive population of new adult corals. For a given species, this population will comprise a critical number of survivors when corals reach reproductive age. Additionally, maximum long-term growth rates will be a factor—the larger the colony, the greater its potential capacity. Controlled field studies with newly metamorphosed agariciids have allowed us, for example, to determine those criteria for species in this complex. One of the lessons from these studies has been how critical it is to determine in pilot studies what type of habitat confers the greatest growth and survivorship for a particular species (Raimondi and Morse forthcoming). As soon as corals become reproductive, relative measures of their reproductive capacity will be the
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP other criteria. When the reef becomes reasonably well established, we would expect to see an influx of fish, particularly those associated with corals rather than macroalgae. Particularly in Florida, transplantation of corals from a healthy coral-rich area to one requiring restoration is being considered as an alternate (but not necessarily competing) approach. Attachment of fragments, or even whole corals, to hard substrates with underwater cement is possible. This approach appears to be a possible viable alternative. There are, however, several considerations, particularly when large areas are to be restored. First it means removing large amounts of coral biomass, whether it be composed of multiple fragments or individual adults, because successful fertilization for any one species depends on a critical number of individual colonies in relatively close proximity to one another. This criterion is true for both mass spawning and planulating corals. Judging from the relatively low success of fertilization in the wild on established reefs compared with that obtained by individual crosses in the laboratory, the required number of colonies is high. The other suggestion to save recently dislodged corals, which involves sending teams of volunteers into the field to transport these corals to an aquaculture facility, also has its limitations. Assuming we had determined the culturing conditions, this approach would work only with rather small corals. Larger corals would overwhelm the capability of most systems to effectively remove the nutrient waste produced by any significant number of larger corals. Rather, it would be better to attempt to cement them back on the reef, even with the inevitable loss of some tissue. We recently removed reattached fragments of Acropora palmata to a variety of sites to monitor differential survival and growth; there were no survivors after 1 month. So far, there have been no success stories using this approach, but it is worth consideration. Molecular Physiology The development of modern technologies for analysis and assessment of the core physiological processes of photosynthesis and symbiosis, reproduction, development, and growth in corals will be required for accurate predictions of stresses that affect corals (Glynn 1993). This type of information is central to successful reef restoration. We need to be able to quickly and efficiently detect and diagnose impending, acute responses of corals to stress that lead to reproductive and recruitment failure, bleaching, and mortality. To date, we have no physiological indicators of impending reduction of the former two processes. Recent studies, however, have identified a number of indicators associated with increased UV radiation and elevated seawater temperatures that result in coral bleaching.
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Induced expression of specific heat-shock proteins has been detected in coral tissues before actual bleaching (Black and others 1995; Fang and others 1997; Hayes and King 1995; Jones and others 1998), as has that of UVB-protectant proteins (Gleason and Wellington 1995) and DNA repair enzymes (Lesser 1996, 1997), the production of which are indicative of high levels of UV radiation. For these proteins and the P-450 proteins induced in response to increased pollution and sediment, we currently have only phenotypic screening to screen for their presence. Earlier detection with increased accuracy is now possible by genotypic screening. Technologies are needed to develop molecular diagnostic indicators using, for example, gene chips as suggested above for exquisite detection of altered gene expression. Deep Reef Corals Recent investigations by myself and other researchers of populations of corals on deeper reef (70-95 m) slopes in the Caribbean suggest that these relatively disturbance-free communities may provide additional insights into the mechanisms that maintain healthy reefs (Bunkley-Williams and others 1988; Fricke and Meischner 1985; Ghiold and Smith 1990; Goreau and Wells 1967). Additionally, particularly in times of high stress in shallower parts of the reef, they may be sources of larvae for natural replenishment of recruits. In this respect, they may be potentially useful candidates for the study of adaptive mechanisms that facilitate coral colonization outside their normal range. Warner (1997) has suggested that corals may be able to vary the phenotypes of their young to adapt to variable environments. Although such investigations may not be for immediate consideration, they are something to consider for the future. REFERENCES Ayre DJ. 1990 Population subdivision in Australian marine invertebrates: Larval connections versus historical factors. Aust J Ecol 15:403-411. Ayre DJ, Hughes TP, Standish RJ. 1997 Genetic differentiation, reproductive mode, and gene flow in the brooding coral Pocillopora damicornis along the Great Barrier Reef, Australia. Mar Ecol Prog Ser 159:175-187. Black NA, Voellmy R, Szmant AM. 1995 Heat shock protein induction in Montastrea faveolata and Aiptasia pallida exposed to elevated temperatures. Biol Bull 188:234-240. Bohonak AJ. 1999 Dispersal, gene flow, and population structure. Q Rev Biol 74:21-45. Brown BE, Dunne RP, Chansang H. 1996 Coral bleaching relative to elevated seawater temperature in the Andaman Sea (Indian Ocean) over the last 50 years. Coral Reefs 15:151-152.
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Buddemeier RW, Smith SV. 1999 Coral adaptation and acclimatization: A most ingenious paradox. Am Zool 39:1-9. Bunkley-Williams L, Morelock J, Williams EH Jr. 1988 Lingering effects of the 1987 mass bleaching in Puerto Rican reefs in mid to late 1988. J Aquat Anim Health 3:242-247. Chadwick-Furman NE. 1996 Reef coral diversity and global change. Global Change Biol 2:559-568. Chen CA, Odorico DM, ten Lohuis M, Veron JE, Miller DJ. 1995 Systematic relationships within the Anthozoa (Cnidaria: Anthozoa) using the 5′-end of the 28S rDNA. Mol Phylogenet Evol 4:175-182. Coll JC, Bowden BF, Meehan GV, Konig GM, Carroll AR, Tapiolas DM, Alino PM, Wheaten A, De Nyse R. 1994 Chemical aspects of mass spawning in corals: I. Sperm-attractant molecules in the eggs of the scleractinian coral Montipora digitata. Mar Biol 118:177-182. Done TJ. 1999 Coral community adaptability to environmental change at the scale of regions, reefs and reef zones. Am Zool 39:66-79. Fang L-S, Huang S-P, Lin K. 1997 High temperature induces synthesis of heat-shock proteins and the elevation of intracellular calcium in the coral Acropora grandis. Coral Reefs 16:127-131. Fisk DA, Done TJ. 1985 Mass bleaching of corals on the Great Barrier Reef. In: Proceedings of the 5th International Coral Reef Symposium 5:149-154. Fricke H, Meischner D. 1985 Depth limits of Bermudan (Atlantic Ocean) scleractinian corals: A submersible survey. Mar Biol 88:175-188. Gerhold D, Rushmore T, Caskey CT. 1999 DNA chips: Promising toys have become powerful tools. Trends Biochem Sci 24:168-173. Ghiold J, Smith SH. 1990 Bleaching and recovery of deep-water, reef-dwelling invertebrates in the Cayman Islands, British West Indies. Carib J Sci 26:52-61. Gleason DF, Wellington GM. 1995 Variation in UV-B sensitivity of planula larvae of the coral Agaricia agaracites along a depth gradient. Mar Biol 123:693-703. Glynn PW. 1993 Coral reef bleaching—Ecological perspectives. Coral Reefs 12:1-17. Glynn PW. 1996 Coral reef bleaching: Facts, hypotheses and implications. Global Change Biol 2:459-509. Goreau T, Wells JW. 1967 The shallow-water scleractinian of Jamaica: Revised list of species and their vertical distribution and range. Bull Mar Sci 17:442-453. Hayes RL, King CM. 1995 Induction of 70-kD heat shock protein in scleractinian corals by elevated temperature: Significance for coral bleaching. Mol Mar Biol Biotech 4:36-42. Hughes TP, Baird AH, Dinsdale EA, Moltschaniwskyj NA, Pratchett MS, Tanner JE, Willis BE. 1999 Patterns of recruitment and abundance of corals along the Great Barrier Reef. Nature 397:59-63.
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Jokiel Pl, Coles SL. 1990 Response of Hawaiian and other Indo-Pacific reef corals to elevated temperature. Coral Reefs 8:155-162. Jones RJ, Hoegh-Guldberg O, Larkum AWD, Schreiber U. 1998 Temperature-induced bleaching of corals begins with impairment of the CO2 fixation mechanism in zoozanthellae. Plant Cell Environ 21:1219-1230. Lesser MP. 1996 Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates. Limnol Ocean 41:271-283. Lesser MP. 1997 Oxidative stress causes coral bleaching during exposure to elevated temperatures. Coral Reefs 16:187-192. McField MD. 1999 Coral response during and after mass bleaching in Belize. Bull Mar Sci 64:155-172. Meesters EH, Bak RPM. 1993 Effects of coral bleaching on tissue regeneration potential and colony survival. Mar Ecol Prog Ser 96:189-198. Morse ANC. 1991 How do planktonic larvae know where to settle? Am Sci 79:154-167. Morse ANC. 1996 Effects of natural bleaching event on agariciid larval production, metamorphosis, overall survival and growth. In: Proceedings of the 8th Coral Reef Symposium, Panama. Morse ANC. 1998 An ancient chemosensory mechanism controls metamorphosis of larvae in divergent coral families. In: Proceedings of the 3rd International Larval Biology Meeting, Melbourne, Australia. Morse ANC, Iwao K, Baba M, Shimoike K, Hyashibara T, Omori M. 1996 An ancient chemosensory mechanism brings new life to coral reefs. Biol Bull 191:149-154. Morse ANC, Morse DE. 1996 Flypapers for coral and other planktonic larvae. BioSci 46:254-262. Morse DE. 1984 Biochemical and genetic engineering for improved production of abalones and other molluscs. Aquaculture 39:263-282. Morse DE, Duncan H, Hooker N, Morse A. 1977 Hydrogen peroxide induces spawning in molluscs, with activation of prostaglandin-endoperoxide synthetase. Science 196:298-300. Morse DE, Hooker N, Morse A. 1978 Chemical control of reproduction in bivalve molluscs. III: An inexpensive technique for mariculture of many species. Proc World Maricult Soc 9:543-547. Morse DE, Hooker N, Morse ANC, Jensen R. 1988 Control of larval metamorphosis and recruitment in sympatric agariciid corals. J Exp Mar Biol Ecol 116:193-217. Morse DE, Morse ANC. 1991a Enzymatic characterization of the morphogen recognized by Agaricia humilis (scleractinian coral). Biol Bull 181:104-122. Morse DE, Morse ANC. 1991b Molecular signals, receptors and genes controlling reproduction, development and growth: Practical applications for improvements in molluscan aquaculture. Bull Inst Zool Acad Sinica Monogr 16:441-454.
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OPPORTUNITIES FOR ENVIRONMENTAL APPLICATIONS OF MARINE BIOTECHNOLOGY: PROCEEDINGS OF THE OCTOBER 5-6, 1999, WORKSHOP Morse DE, Morse ANC, Raimondi PT, Hooker N. 1994. Morphogen-based chemical flypaper for Agarica humilis coral larvae. Biol Bull 186:172-181. Raimondi PT, Morse ANC. The consequences of complex larval behavior in a coral. Ecology (Forthcoming). Richmond RH. 1987 Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis. Mar Biol 93:527-533. Rinkevich B. 1996 Do reproduction and regeneration in damaged corals compete for energy allocation? Mar Ecol Prog Ser 146:297-302. Romamo SL, Palumbi SR. 1996 Evolution of scleractinian corals inferred from molecular systematics Science 271:640-642. Sammarco PW, Andrews JC. 1988 Localized dispersal and recruitment in great Barrier Reef corals: The Helix experiment. Science 239:1422-1424. Smith SV, Buddemeier RW. 1992 Global change and coral reef ecosystems. Ann Rev Ecol Sys 23:89-118. Szmant AM, Glassman NJ. 1990 The effects of prolonged bleaching on the tissue biomass and reproduction of the reef coral ontastrea annularis. Coral Reefs 8:217-224. Tarrant AM, Atkinson S, Atkinson MJ. 1999 Estrone and estradiol-17 beta concentrations in tissue of the scleractinian coral Montipora verrucosa. Comp Biochem Physiol 122:85-92. Veron JEN, Odorico DM, Chen CA, Miller DJ. 1996 Reassessing evolutionary relationships of scleractinian corals. Coral Reefs 15:1-9. Warner RR. 1997 Evolutionary ecology: How to reconcile pelagic dispersal with local adaptation. Coral Reefs 16:115-120. Wilkinson C, Linden O, Caesar H, Hodgson G, Rubens J, Strong AE. 1999 Ecological and socioeconomic impacts of 1998 coral mortality in the Indian Ocean: An ENSO impact and a warning of future change? AMBIO 28:111-196.
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