Introduction

I had planned on writing the second part to the Dominican coral farm article this month, but have not been in the same frame of mind to continue the "fun" tone of the first part of that article. So, rather than force the mindset, I have decided to engage in a two-part article I have been planning for longer than a few years. For many years, I have been accumulating reports of spawning in aquarium corals. I have always felt this to be one of the ultimate goals in captive reef husbandry, and have written many times that our success in coral husbandry will be, to a great degree, measured by the number and predictable nature of occurrences of sexual reproduction. Until relatively recently, coral spawns in aquaria were sporadic events and without any regularity or periodicity. For the most part, this is still true, but reports are becoming more and more frequent, and in relatively new tanks cared for by persons without extensive experience with reef tanks. To me, this is significant.

Finally, and perhaps most importantly, for at least some of the spawning events being reported and photographed in aquariums, what is being witnessed is truly novel. First, for some events, it is reproduction of a species that has never been witnessed, documented, or known in the wild and serves as an important observation for general understanding of the nature of sexual reproduction in that species. Second, for at least a few species that have spawned in aquariums, the method of reproduction seems to be entirely different than what has been observed or documented in the wild. This is, to say the least, very interesting.

I will begin this month with an overview of sexual reproduction in corals, and continue next month with a very long and photo-heavy documentation of coral spawning events in aquariums, including how these spawns are either similar or different to what is known about them in the wild.

Sexual Reproduction of Corals on Reefs

Reproduction and recruitment of corals on coral reefs is one of the most critical processes that allows for the persistence of coral reefs over geological time frames. Corals reproduce both sexually and asexually. Many corals are able to spread across reef space by asexual means, such as fragmentation, but this results in clones of the same colony and does not increase the diversity or gene pool of the reef. If all corals spread by fragmentation or other asexual means, reefs may have long ago ceased to exist, or at least be very different, perhaps becoming victims of inbreeding depression and a few monospecific stands competing with each other, with one or a few likely to eventually achieve spatial dominance.

Sexual reproduction requires the fusion of male and female gametes (sperm and egg) that form a zygote which grows into an embryo that develops into a free-swimming larva called a planula. Eggs and sperm are produced in accumulations of gastrodermal tissue (the innermost of the two coral tissue layers) on the mesenteries called ovaries and spermaries, respectively. Planulae are highly variable between species, and some have the capacity to exist in the plankton for long periods (over 100 days in some species); this allows for long-distance dispersal and the potential ability of corals to seed reefs far away from the parent colony. Thus, by reproducing sexually, there is genetic diversity acquired by: 1) the contributions of both male and female sex cells from colonies; 2) meiotic cross-over events during the formation of those sex cells; and 3) increases in the community genetic pool by having new colonies recruit from outside the local community through dispersal of planulae. This has practical implications in that reefs which might be lost to natural or man-made catastrophes will still persist in that the gene pool of colonies might exist far away, and that in time, the gene pool of reefs far away can reseed the reef that has been destroyed.

The "Sexual Orientation" of Corals

No, this is not a joke that demands political correctness. Corals can be divided into two major groups in regard to their sexual nature.

The first group is divided into two subgroups depending on whether or not a colony produces separate sperm and eggs. Gonochoric (also known as dioecious) species, or those in which colonies are either male (producing sperm) or female (producing eggs), comprise about 25 percent of corals studied. The remaining 75 percent are considered hermaphroditic, where a single colony produces both sperm and eggs. The term hermaphrodite is interesting; it comes from Greek mythology. Hermes was the messenger of the gods, and Aphrodite was the goddess of beauty. Hence, the male sperm "messenger" delivers his package to the female egg "beauty goddess." Six species, Agarcia agaracites, A. humilis, Galaxea fascicularis, G. astreata, Caryophyllia ambrosia, and Porites astreoides, have been reported as having the potential to be either gonochoric or hermaphroditic.

Hermaphroditism can be further subdivided into three other groups. In the first, simultaneous hermaphrodites, sperm and eggs are produced at the same time. Other species are functional male colonies first, and then develop into functional female colonies. This is called protandry. On the other hand, some species are functional female colonies first, and then develop into functional male colonies. This is called protogyny. Species that are either protandrous or protogynous are called sequential hermaphrodites. The majority of hermaphroditic corals are simultaneous hermaphrodites.

The second group is divided into two subgroups depending on how gametes come into contact with each other. Broadcast spawners release eggs and sperm into the water column for external fertilization and development. Brooders have eggs fertilized internally with development of the planulae within the polyps. The majority of corals studied are broadcast spawners (approximately 85 percent), with the remaining 15 percent being brooders. Until recent times, it was believed that most corals were "viviparous," or brooders. Notably contrary to most animals, some coral species, such as Pocillopora damicornis, are known to exhibit both brooding and broadcast spawning reproductive methods in different locations. It has also been proposed that this may be a valid reason to examine such populations to see if they are really separate species or subspecies.

The Importance of Being Different

The variations in sexual reproduction in corals are theoretically significant in numerous ways. To better understand the importance of these traits, each method has various characteristics that can be generally applied to the species or communities utilizing them. In terms of hermaphroditic and gonochoric species, hermaphroditism is favorable in small populations so that there an increased likelihood of having successful fertilization. Even one simultaneous hermaphrodite can produce many new planulae and still not suffer from significant inbreeding because of crossing-over events during meiosis. Each polyp in a colony undergoes separate cross-over events in the production of gametes, and so a colony of several thousand, or even million, polyps can theoretically produce half that number of viable, genetically different colonies all by itself.

This feat has several important implications. First, it makes it apparent how effective corals can be in terms of keeping reefs populated and is certainly a major reason for their success over eons of time. Second, it is testimony to the advantages of both hermaphroditism and a colonial lifestyle. Third, it should be apparent how advantageous it could be in terms of producing all the corals ever required for the aquarium trade by having sexual reproduction occur and a means to settle and rear the recruits. Quite literally, one or two colonies of a species could provide for every coral ever demanded by the aquarium trade forever. In other words, were a person so inclined, a thousand coral colonies of different species could be the sum impact that the aquarium coral trade has on reefs from now on and still provide the same diversity of species available and be continuously available. In contrast, some one million coral colonies will be taken from coral reefs this year to supply just the United States aquarium trade, most of which will not survive and, of the survivors, most of which will never reproduce.

The major difference in the life history of corals is not between gonochorism and hermaphroditism, however, it is in the differences between brooding and broadcast spawning. These differences include the transfer of zooxanthellae to the larvae, larval dispersal times, dispersal patterns, genetic variability and rates of speciation and evolution.

Brooders produce planula larvae that, when released, are immediately competent to settle and metamorphose into juveniles. They are generally larger than the larvae produced by non-brooders, and contain a "starter culture" of zooxanthellae. As such, they tend to not disperse for long or very far, and the larvae of brooders tend to settle and metamorphose usually close to the parent or within the same local community. It is interesting that although brooded planulae are potentially able to disperse farther because of the zooxanthellae providing them with energy, they generally do not do so. Not all brooders develop the planulae within the gastric cavity of the polyp, either. At least some species brood the larvae on the surface of the colony, underneath the mucus; soft corals, such as Clavularia and Briareum (star polyps) are known to engage in surface brooding.

Broadcast spawners, in contrast, fertilize externally, and the planulae develop in the water column. The length of time it takes for them to develop competence to settle depends on the species, and can also depend on environmental cues. This time can vary between hours to weeks. Because sperm and egg are separate and fertilize external to the parent polyp, zooxanthellae must be acquired from the water column. Depending on the time of zooxanthellae acquisition, and the specific characteristics of a species planulae, the pelagic phase for broadcast spawning corals prior to becoming competent to settle can last from less than a day to over 120 days. Broadcast spawning corals tend to settle and metamorphose away from local communities, but are thought to usually settle no farther than nearby communities (with obvious potential to go farther). However, this aspect has rarely been even attempted to be measured as it is very difficult to track individual planulae in a pelagic state.

The Magic of Being a "Synchronous, Simultaneous, Hermaphroditic, Broadcast Spawning Colonial Coral Species."

What a mouthful of verbiage! As will be discussed in more detail below, broadcast spawners often release en masse, otherwise known as synchronous mass spawning; that is, within a period of hours to days, many species release their gametes synchronously. This is called swamping, and is thought to maximize the number of successful fertilizations be reducing he number of eggs that predators could consume by overloading their abilities to consume them all. Most simultaneous coral hermaphrodites do not release eggs and sperm separately, but release them in egg-sperm packets, with a few to several hundred eggs surrounding (or surrounded by) a packet of sperm. After several minutes to hours, and depending sometimes on environmental cues, the packets rupture and fertilization can take place. This is important, because eggs are positively buoyant and will float to the surface, and they have fairly long competency periods in seawater. Sperm, however, are rapidly diffused in water, are not buoyant, and have a short competency period in seawater. Were eggs and sperm not released exactly at the same time, and if fertilization did not take place in the immediate vicinity of the colony, a much lower fertilization success rate would likely occur. Because both eggs and egg-sperm packets float, they form slicks on the water surface that can drift for many days and many miles. As this mass of gametes drifts, and as the egg-sperm packets rupture, there is a much greater chance of fertilization taking place, and a much greater chance of genetic mixing. Furthermore, because planulae from broadcast spawners can disperse farther, they tend to persist longer over evolutionary time frames. This probably accounts for the fact that most corals are synchronous, simultaneous hermaphroditic broadcast spawners. The success rate for fertilization and maintenance of the species gene pool and metapopulation is the highest.

Synchronicity

Much attention has been given to the factors that result in the almost mystical synchronous mass spawning that occurs on coral reefs around the world. I must preface by saying a few things: First, not all corals, nor all coral reefs, have mass spawning events; Second, not all corals, nor all coral reefs, spawn at the same time; Third, not all coral or coral reefs seem to depend on the same cues for mass spawning. The first mass spawning event was not even officially "discovered" until the early 1980's! Since then, and with more and more divers and researchers in the waters, it is becoming clear that many, if not most, corals on reefs participate in these amazing events. For anyone interested, the video, Coral Sea Dreaming, has outstanding footage of mass spawning on the Great Barrier Reef that involves corals, sea stars, sea cucumbers, and polychaetes in an underwater display that is too beautiful to even describe.

As prefaced above, and perhaps to the chagrin of many aquarists, the exact cues that are involved in mass spawning are not fully understood. Many aquarists erroneously believe that they will trigger mass spawning in their aquaria by putting a "moonlight" bulb above their tanks. Unfortunately, I fear this will not do much. What follows below is a summary of what seems to be the general sequence of events required for corals to mature and release their gametes.

Corals, like other organisms, take time to reach reproductive maturity. Unlike humans, there is no set period before and during "puberty." For some species, age seems to be the determining factor; for example, Xenia species have been found to become reproductively mature at about one year of age while female colonies of Sarcophyton spp. may be ten to twelve years old before they mature. For other species, it appears that a set size must be reached before the colony becomes reproductively mature. For some corals, they must have a surface area that exceeds a certain critical size, while for others it may be branch length. For still other species, it appears that polyp density may be the determining factor for sexual maturity; that is, once a certain number of polyps have been formed, the colony can begin producing gametes irrespective of the surface area of the colony or the length of the branches - processes that become confounded by aspects of growth such as calcification rates, growth forms, and skeletal density.

It is worth mentioning that though a colony may be of a correct age, size, or polyp density, that there is no guarantee that the colony is or will become fecund (capable of producing offspring). Production of gametes requires a large amount of energy, and a spawning coral may release 25-75% of its biomass during spawning. Thus, production of gametes requires a significant surplus of energy beyond that required for metabolism and growth. During gametogenesis, it has been found that many corals may also stop feeding, so that excess must be acquired prior to commencement of gamete formation, and from that acquired by photosynthesis in zooxanthellate corals. However, gametes are protein rich, and so photosynthesis may be more important for simply maintaining the coral during half the year while it is producing ripe gonads, rather than for any major contribution to the gonads directly. Furthermore, any stress, injury, or partial colony mortality may either sap enough energy such that gamete production is halted and gametes resorbed, or it may drop the colony to a size or polyp density below the minimum required for reproduction. In some cases, a colony may be partially fecund, with large expansive healthy areas of the colony releasing gametes with less healthy areas not having fecund polyps.

It is thought that temperature plays the prominent role in signaling for gonad and gamete production. Generally, as temperatures begin to warm, gonads begin to ripen. This process may take half a year or more, and areas with variable or very stable year-round water temperatures present somewhat of a mystery. It is also notable that the winter is a time of reduced growth in corals and early spring often a time of increased plankton abundance. Perhaps corals use this time to amass the nitrogen-rich food required for the time of gonad production occurring during the summer. This maturation process is typical for most reef corals in that the majority seem to have annual spawning events. However, many reefs and corals may spawn biannually or semiannually, and some corals may also spawn on a monthly cycle. This clearly indicates that more must be learned about spawning behavior in corals. On the other hand, anomalous years with regard to temperature often result in spawning events that do not take place on the expected month, or they may not occur at all that year. This lends some additional credence to the role of water temperature in sexual maturation of reef corals.

As water temperatures reach their annual maxima, the gametes are produced by the now mature ovaries and spermaries and reside within the corals until a triggering event causes their release. As indicated above, spawning typically takes place on the month of, or the month after, the warmest average monthly water temperature in annual mass spawnings. However, the "fame" of mass spawning events is related to lunar periodicity. It is thought that the lunar phase provides the cues for the timing of mass gamete release. In other words, during the month of the hottest water temperature, the day and time of the release depends on the phase of the moon. It was thought, based on early reports of limited mass spawning sites, that spawning occurred a night or two after the full moon. However, with more reports and documentations, spawning may be highly correlated to a lunar phase, but varies significantly across locations. It makes most sense that release should take place when the moon is new and the waters are darkest to minimize loss of eggs by predation. However, I am not aware that any real patterns have emerged as to the exact lunar phase that incorporates any real majority of reefs. Unfortunately for aquarists whose corals likely came from many different reefs, the use of a moonlight, even if cyclically dimmed, will probably not have much of an effect in triggering mass spawns in a tank, even if the tank has been temperature controlled for seasonal cycles, and even if the corals are sexually mature and fecund.

Furthermore, chemical cues are involved in spawning and mass spawning events, although the exact cues and factors are only beginning to be discovered. Sperm attractants have been isolated in a number of species, and such water borne signals may be important in triggering spawning in other species. In addition, a number of other factors have been proposed or determined to be contributing to, or being responsible for, various aspects of spawning behavior. A list of the many factors involved in coral spawning is found in Table 1.

In particular, one area in which I believe deserves more study was proposed as a result of annual and synchronized mass spawning in corals from the Red Sea where temperature variation over the year was highly variable. Coral polyps are unable to detect light levels, and it is the zooxanthellae that are able to detect light. However, there is considerable question as to the ability of these intracellular algae to detect changes in photon flux density that is on the scale of the irradiance levels of moonlight, even on a full moon. Zooxanthellae reside within coral tissue of varying thickness and opacity, under a variably thick mucus layer containing variable levels of other photosynthetic microbes and receive a mere fraction of the light reaching the coral surface. Depth, turbidity, haze in the air, clouds, over flights of Israeli aircraft, or any number of exceptionally minor events could change the irradiance levels of moonlight to an extent that in all likelihood makes it almost impossible to even remotely consider the possibility that zooxanthellae or corals could detect whether or not a particular night is a full moon or a new moon. Furthermore, spawning events will often, though not always, happen irrespective of how cloudy or hazy the night of the spawn might be, or how turbid or deep the water, or how shaded a colony might be by another. For an organism to have a biological response to light requires a photoreceptor and an immediate and quantifiable response for its nervous system. In corals the only photoreceptors are the zooxanthellae, and their response, the production of photosynthetically-produced chemicals, is neither specific enough nor quantitative enough for such a use.

However, and as the study mentioned above suggested, there is one factor that will not vary annually and involved light levels and periods which would be detectable by zooxanthellae - day length or night length. Terrestrial plants are triggered to flower, fruit or produce fall colors based on whether they are long day (short night), intermediate day, or short day (long night) plants. In other words, when day length or night length reaches a critical value, phytochromes trigger signal transduction processes that cause hormones and other signals to be produced that, in turn, cause behavioral and biochemical processes. It is my feeling that future research will find that zooxanthellae are responsible for triggering the coral polyp's gamete release by producing chemical signals based on day or night length. However, there is still a question remaining. There are day-neutral plants that do not respond to changes in day or night length, and they are primarily tropical ones where there is little or no variation in day length. They must depend on other proximate cues that may vary between species. However, this likely explains the variations in timings of mass spawning events on various reefs, why moonlight levels have not been found to have a strong correlation across reefs, and perhaps, most interestingly, why equatorial reefs seem to have less predictable (or semi-annual) mass spawning events than those at higher latitudes. To my knowledge, this idea is not being pursued in the coral research community but deserves investigation.

The Timing of Gamete Release

In general, corals release their gametes at night, although there are many examples of daytime release and some, such as Fungia species, may spawn day and night. Most spawning takes place over a period of minutes to hours, although release may be spread out over several consecutive nights. In rare cases, such as with Hydnophora exesa, spawning may be spaced out over several weeks. The timing of release is usually consistent from year to year; so much so that the spawning times of coral species can be predicted within a matter of minutes. For example, in the Flower Gardens, Diploria spawns between 9:00 and 10:00 p.m. and Montastraea spawns fifteen to thirty minutes later, followed an hour later by Stephanocoenia. This predictability in the degree of timing by at least the initial coral species is absolutely astonishing, although species following may be reacting to chemical cues.

Settlement and Metamorphosis - Only the Beginning

Upon successful formation of competent planulae, either by brooding or by fertilization in the water column of broadcast spawning corals, there are events that determine if and where the planulae will settle on the reef, and then metamorphose into a juvenile coral polyp. To date, a number of factors have been proposed to explain the environmental cues required to initiate the planulae descending from the water column to settle on substrate. Among the most studied are rugosity (roughness) of the substrate, depth, light, biofilms produced by bacteria and other microorganisms, and coralline algae. Current thought and research suggests that coralline algae are by far the most important factor involved. Specific chemical signals have been isolated from coralline algae that induce settlement in coral and other invertebrate larvae with controls for depth, light, and biofilms indicating they play secondary, if any roles, in the event. The variations reported for the other factors are easily explained in that various coralline algae produce different chemical signals, are variable in the depths they inhabit, have different associated biofilms, and may grow preferentially on substrates of varying rugosity.

Once settled on coralline algae, planulae tend to settle in protected areas and crawl outwards into the light over a varying period of time that probably reflects a degree of competence in the metamorphosis process that ensures the newly settled spat are in an optimal position for survival and reflects their ability begin calcifying, as well as to have access to food, light, and space. Some coral species, such as Pocillopora damicornis, produce larvae that can and do release from their settlement site if conditions are not optimal and resettle at a later time (if available substrate exists!), indicating that the settlement and metamorphosis processes are both dynamic and not inflexible. Following settlement and metamorphosis, a tiny single coral polyp faces a very uncertain period where mortality rates are extremely high. However, if successful, this tiny almost unrecognizable polyp may, over the course of years to centuries, become a coral colony capable by itself of reseeding countless other coral reefs perhaps thousands of miles away - most remarkable life history story and biological adventure.

In the next column, the marvel of nature described in this article will be furthered in describing even more remarkable events…coral spawning in captive reef aquaria.

Link to Part II

References:

Review articles are highlighted in red.

Babcock, R. C. (1984). "Reproduction and distribution of two species of Goniastrea (Scleractinia) from the Great Barrier Reef province." Coral Reefs 2: 187-195.

Baird, A. H. and R. C. Babcock (2000). "Morphological differences among three species of newly settled pocilloporid coral recruits." Coral Reefs 19: 179-183.

Ben-David-Zaslow, R., G. Henning, et al. (1999). "Reproduction in the Red Sea soft coral Heteroxenia fuscescens: seasonality and long-term record (1991 to 1997)." Marine biology 133: 553-559.

Benayahu, Y. (1992). Onset of zooxanthellae acquisition in course of ontogenesis of broadcasting and brooding soft corals. Proceedings of the Seventh International Coral Reef Symposium, Guam, University of Guam Press.

Benayahu, Y., Y. Achituv, et al. (1988). "Embryogenesis and acquisition of algal symbionts by planulae of Xenia umbellata (Octocorallia: Alcyonacea)." Marine Biology 100: 93-101.

Benayahu, Y., T. Berner, et al. (1989). "Development of planulae within a mesogleal coat in the soft coral Heteroxenia fuscescens." Marine Biology 100: 203-210.

Benayahu, Y. and Y. Loya (1983). "Surface brooding in the Red Sea soft coral Paraerythropodium fulvum fulvum (Forskal, 1775)." Biological Bulletin 165: 353-369.

Benayahu, Y. and Y. Loya (1984). "Life history studies on the Red Sea coral Xenia macrospiculata Gohar, 1940. I. Annual dynamics of gonadal development." Biological Bulletin 166: 32-43.

Benayahu, Y. and Y. Loya (1984). "Life history studies on the Red Sea coral Xenia macrospiculata Gohar, 1940. II. Planulae shedding and post larval development." Biological Bulletin 166: 44-53.

Benayahu, Y. and Y. Loya (1986). "Sexual reproduction of a soft coral: synchronous and brief annual spawning of Sarcophyton glaucum (Quoy & Gaimard, 1833)." Biological Bulletin 170: 32-42.

Benayahu, Y. and M. H. Schleyer (1998). "Reproduction in Anthelia glauca (Octocorallia: Xeniidae). II. Transmission of algal symbionts during planular brooding." Marine Biology 131: 433-442.

Benayahu, Y., D. Weil, et al. (1992). "Entry of algal symbionts into oocytes of the coral Litophyton arboreum." Tissue and Cell 24(4): 473-482.

Bowden, B., J. Coll, et al. (1985). Some chemical aspects of spawning in Alcyonacean corals. Proceedings of the Fifth International Coral Reef Symposium, Tahiti.

Brazeau, D.A., and H. R. Lasker. 1990. Sexual reproduction and external brooding by the Caribbean gorgonian Briareum abestinum. Mar Biol 104: 465-74.

Brazeau, D.A., and H.R. Lasker. 1989. The reproductive cycle and spawning in a Caribbean gorgonian. Biol Bull 176: 1-7.

Carleton, J. H. and P. W. Sammarco (1987). "Effects of substratum irregularity on success of coral settlement: quantification by comparative geomorphological techniques." Bulletin of Marine Science 40(1): 85-98.

Chen, C.A., et. al. 1995. Sexual and asexual reproduction of the tropical Corallimorpharian Rhodactis (=Discosoma) indosinensis (Cnidaria: Corallimorpharia) in Taiwan. Zool Stud 34: 29-40.

Coffroth, M. A. and H. R. Lasker (1998). "Larval paternity and male reproductive success of a broadcast-spawning gorgonian, Plexaura kuna." Marine Biology 131: 329-337.

Coll, J. C., B. F. Bowden, et al. (1990). "Chemistry and coral reproduction." ___in Britain: 760-763.

Cooke, William J. 1976. Reproduction, growth, and some tolerances of Zoanthus pacificus and Palythoa vestitus in Kaneohe Bay, Hawaii. In: Coelenterate Ecology and Behavior (Mackie, ed.) University of Victoria, British Columbia. pp. 281-8.

Dahan, M. and Y. Benayahu (1997). "Reproduction of Dendronephthya hemprichii (Cnidaria: Octocorallia): year-round spawning in an azooxanthellate soft coral." Marine Biology 129: 573-579.

Fadlallah, Y. H. (1983). "Sexual reproduction, development and larval biology in scleractinian corals." Coral Reefs 2: 129-150.

Fadlallah, Y. H. (1996). "Synchronous spawning of Acropora clathrata coral colonies from the western Arabian Gulf (Saudi Arabia)." Bulletin of Marine Science 59(1): 209-216.

Fadlallah, Y. H. and R. T. Lindo (1988). Contrasting cycles of reproduction in Stylophora pistillata from the Red Sea and the Arabian Gulf, with emphasis on temperature. Proceedings of the 6^th International Coral Reef Symposium, Australia.

Fan, T.-Y. and C.-F. Dai (1998). "Sexual reproduction of the sclerctinian coral Merulina ampliata in southern Taiwan." Bulletin of Marine Science 62(3): 897-904.

Fiene-Severns, P. (1998). A note on synchronous spawning in the reef coral Pocillopora meandrina at Molokini Islet, Hawaii., University of Hawaii.: 4.

Glynn, P. W., S. B. Colley, et al. (1994). "Reef coral reproduction in the eastern Pacific: Costa Rica, Panama, and Galapagos Islands (Ecuador). II. Poritidae." Marine Biology 118: 191-208.

Goffredo, S., S. Arnone, et al. (2002). "Sexual reproduction in the Mediterranean solitary coral Balanophyllia europaea (Scleractinia, Dendrophylliidae)." Marine Ecology Progress Series 229: 83-94.

Hall VR, Hughes TP. 1996. Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77: 950-963.

Harriott, V. J. (1983). "Reproductive ecology of four scleractinian species at Lizard Island, Great Barrier Reef." Coral Reefs 2: 9-18.

Harrison, P.L., and C.C. Wallace. 1990. Reproduction, dispersal, and recruitment of scleractinian corals. In: Coral Reefs: Ecosystems of the World Vol 25 (Z. Dubinsky, ed.). Elsevier Scientific Publishing Co. Inc. New York: 133-208.

Harrison, P., R. Babcock, et al. "Recent developments in the study of sexual reproduction in tropical reef corals." 217-219.

Harrison, P. L. (1988). Psuedo-gynodioecy: an unusual breeding system in the scleractinian coral Galaxea fascicularis. Proceedings of the 6^th International Coral Reef Sympsoium, Australia.

Harvell CD, Grosberg RK. 1988. The timing of sexual maturity in clonal organisms. Ecology 69: 1855-1864.

Hines AH. 1986. Larval problems and perspectives in life histories of marine invertebrates. Bull Mar Sci 39: 506-525.

Heyward, A. J. and R. C. Babcock (1986). "Self- and cross-fertilization in scleractinian corals." Marine Biology 90: 191-195.

Hirose, M., R. A. I. Kinzie, et al. (2000). "Early development of zooxanthellae-containing eggs of the corals Pocillopora verrucosa and P. eydouxi with special reference to the distribution of zooxanthellae." Biological Bulletin 199(August): 68-75.

Hodgson, G. (1988). Potential gamete wastage in synchronously spawning corals due to hybrid inviability. Proceedings of the 6^th International Coral Reef Symposium, Australia.

Hunter, C. L. (1988). Environmental cues controlling spawning in two Hawaiian corals, Montipora verrucosa and M. dilatata. Proceedings of the 6^th International Coral Reef Symposium, Australia.

Jokiel, P. L. (1985). Lunar periodicity of planula release in the reef coral Pocillopora damicornis in relation to various environmental factors. Proceedings of the Fifth International Coral reef Congress, Tahiti.

Jokiel, P. L., R. Y. Ito, et al. (1985). "Night irradiance and synchronization of lunar release of planula larvae in the reef coral Pocillopora damicornis." Marine Biology 88: 167-174.

Kruger, A., M.H. Schleyer, and Y. Benayahu. 1998. Reproduction in Anthelia glauca (Octocorallia: Xeniidae). I. Gametogenesis and larval brooding. Mar Biol 131: 423-32

Krupp, David A. 1983. Sexual reproduction and early development of the solitary coral Fungia scutaria (Anthozoa: Scleractinia). Coral Reefs 2: 159-64

McFadden, C. S. (1991). "A comparative demographic analysis of clonal reproduction in a temperate soft coral." Ecology 72(5): 1849-1866.

Omori, M., H. Fukumi, et al. (2001). "Significant drop of fertilization of Acropora corals in 1999: an after-effect of heavy coral bleaching." Limnology and Oceanography 46(3): 704-706.

Richmond, Robert H. and Cynthia L. Hunter. 1990. Reproduction and recruitment of corals: comparisons among the Caribbean, the Tropical Pacific, and the Red Sea. Mar Ecol Prog Ser 60: 185-203.

Richmond, Robert H. 1988. Competency and dispersal potential of planula larvae of a spawning versus a brooding coral. Proc 6^th Int Coral Reef Sym 2: 827-32.

Richmond, Robert H. 1997. Reproduction and recruitment in corals: Critical links in the persistence of reefs. In: Life and Death of Coral Reefs, (Charles Birkeland, ed.). Chapman & Hall, New York: 175-97.

Richmond, Robert H. 1987. Energetic relationships and biogeographical differences among fecundity, growth and reproduction in the reef coral Pocillopora damicornis. Bull Mar Sci 41: 594-604.

Richmond, Robert H. 1985. Reversible metamorphosis in coral planula larvae. Mar Ecol Prog Ser 22:181-5.

Richmond, Robert H., and Paul L. Jokiel. 1984. Lunar periodicity in larva release in the reef coral Pocillopora damicornis at Enewetak and Hawaii. Bull Mar Sci 34: 280-7.

Rinkevich, B., and Y. Loya. 1985. Intraspecific competition in a reef coral: effects on growth and reproduction. Oecologia 66: 100-5.

Rinkevich, B. (19891). "The contribution of photosynthetic products to coral reproduction." Marine Biology 101: 259-263.

Sier, C.J.S., and P.J.W. Olive. 1994. Reproduction and reproductive variability in the coral Pocillopora verrucosa from the Republic of Maldives. Mar Biol 118: 713-22.

Soong, K. 1992. Reproduction and coral size of reef coral species. Proc 7^th Int Coral Reef Sym 1: 503.

Stimson, John S. 1976. Reproduction of some common Hawaiian reef corals. In: Coelenterate Ecology and Behavior, (Mackie, ed.) University of Victoria, British Columbia. pp. 271-80.

Tanner, J.E. 1996. Seasonality and lunar periodicity in the reproduction of pocilloporid corals. Coral Reefs 15: 59-66.

Tomascik, T. and F. Sander (1987). "Effects of eutrophication on reef-building corals II. Reproduction of the reef-building coral Porites porites." Marine Biology 94: 77-94.

Ward, S. (1992). "Evidence for broadcast spawning as well as brooding in the scleractinian coral Pocillopora damicornis." Marine Biology 112: 641-646.

Ward, S. 1995. Two patterns of energy allocation for growth, reproduction and lipid storage in the scleractinian coral Pocillopora damicornis. Coral Reefs 14: 87-90.

Ward, Selina. 1995. The effect of damage on the growth, reproduction and storage of lipids in the scleractinian coral Pocillopora damicornis (Linnaeus). J Exp Mar Biol Ecol 187: 193-206.

Yamazato, K., M. Sai, and Y. Nakano. 1992. Sexual reproduction of Okinawan corals, Stylophora pistillata (Esper) and Seriatopora hystrix (Dana). Proc 7^th Int Coral Reef Sym 1: 504.

Yamazato, Kiyoshi, Mayumi Sato, and Hideyuki Yamashiro. 1981. Reproductive biology of an alcyonarian coral, Lobophytum crassum Marenseller. Proc 4^th Int Coral Reef Sym 2: 671-8.