The husbandry of exotic marine species has seen dramatic changes over the past decades. In the 1950's, pioneers such as Lee Chin Eng still experimented with seaweeds and air stones, which have now been upgraded to computerised aquaria equipped with strong lighting, protein skimmers, calcium reactors and coolers. Nowadays, the husbandry of many coral and other invertebrate species has risen to a high level, allowing for high survival and growth. The next step however, reproduction, remains a major hurdle for most marine species. Sexual reproduction is a key step in the husbandry of any species, as it generates genetic diversity. Closing the life cycle of corals is one of the main future challenges for marine aquarists.

Currently, large numbers of fish, coral and other invertebrate species are exported annually for the American, European and Japanese markets. This trade however is far from sustainable. According to a recent UNEP-WCMC report, only 1% of exported corals has been raised by mariculture or aquaculture¹. This poses yet another challenge for coral reefs, aggravating current issues such as pollution, overfishing, habitat destruction, global warming and ocean acidification.

Figure 1: Culturing corals in captivity will become increasingly important in the future. An increasing number of zoos and public aquaria is growing corals behind the scenes (photograph: Tim Wijgerde, NAUSICAA, Boulogne-sur-mer, France).

The aquaculture of countless marine (in)vertebrate species will have to be upscaled significantly over the following years, due to persisting demand for livestock. Quotas of wild-caught specimens, either corals or fish, will have to be reduced to prevent permanent ecological damage to coral reefs. This change towards a more sustainable approach is already ongoing, and aquarium hobbyists play an important role in this process. Species such as clownfish and sea horses are bred regularly by specialists, who devote a great deal of time to this. Many corals are being fragmented and traded on internet fora and events, and this has led to many commonly available species in the trade. Biologically speaking, fragmentation of corals is a form of vegetative, or asexual reproduction.

Asexual reproduction

A marine aquarium which runs optimally quickly becomes a victim of its own success. Some corals grow out to impressive proportions, after which the colonies are subject to enthusiastic pruning. Fragmenting and selling ramets is a nice way to recuperate some of the investments made, and also allows for expansion of a captive coral population.

"Fragmentation of corals is a form of vegetative, or asexual reproduction."

In the wild, corals are also fragmented constantly; predators and storms continuously break off fragile colonies. Corals also release parts of their colonies, a process called autotomy. This often occurs during periods of stress, and is observed frequently in aquaria. Autotomy can be regarded as a last resort for the colony to survive, in the form of a released part which often completely regenerates.

Corals employ many different strategies of asexual reproduction, including intratentacular budding, extratentacular budding, "dripping", polyp bailout and the formation of anthocauli displayed by members of the Fungiidae family.

Figure 2: Fungia or mushroom corals display an unusual form of asexual reproduction; the formation of numerous daughter colonies from a dying parent polyp. This strategy serves as a last resort, and ensures the survival of the parent polyp (photograph: Jorick Hameter).

Although regular manipulated coral fragmentation is a sign of success, there are disadvantages however. Not only are these colonies prevented from reaching their natural sizes, fragmenting them may also lead to weakened colonies in the long run. Why is this? This has everything to do with genetics.

A coral ramet is an exact genetic copy of its parent colony, and is thus considered a clone. Clones behave exactly the same under equal circumstances, which means they are equally strong, but also equally weak as their parent colonies. Imagine a large Acropora colony sensitive to salinity fluctuations being fragmented into several small colonies. When these fragments are aquacultured, this latent weakness will present itself sooner or later. If these fragments are utilized for reef restoration, and placed near an estuary, success may be limited. This happens when latent weaknesses become apparent too late. The same principle can be applied to corals sensitive to bacterial or parasitic infections, temperature fluctuations or high irradiance levels.

"A coral fragment is an exact genetic copy of its parent colony, and is thus considered a clone. Clones behave exactly the same under equal circumstances."

These problems occur when corals display equal characteristics; this is called a genetically homogeneous population. It is the diversity of characteristics which bestows fitness upon a population of individuals, and this is called a genetically heterogeneous population. A  population of coral colonies with different resistant qualities will therefore have a higher chance of survival in the long run. This is because for each disturbance, it is likely that several individuals will survive as they have an innate resistance to it. A genetically diverse population increases the chances of survival for any given species. There is only one natural way of generating diversity, and that is through sexual reproduction.

Sexual reproduction

Sexual reproduction involves the fusing of gametes, or eggs and sperm, thereby generating a new individual. Gametes are produced by meiosis, which involves separation of chromosomes into new daughter cells. These chromosomes, also called DNA, contain genes which encode proteins having essential functions in life. The overall genetic makeup of any individual therefore determines its characteristics. When eggs and sperm fuse, they generate new combinations of genes, thereby creating a completely unique individual. This process eventually creates a genetically diverse population, with individuals able to respond to a wide array of disturbances. The starting population should of course be sufficiently large, to prevent too much "recycling" of the same genes. Corals produce gametes as well, and when starting out with several hundreds of colonies, a gene pool may be maintained which is reasonably diverse. Collecting "fresh" specimens from the wild every now and then may serve to enrich such a gene pool.

Of course, sexual reproduction sometimes yields weak individuals, when genetic defects or weaknesses are passed on. This is especially true if two or more weaknesses are transferred by both parent colonies to one individual, such as sensitivity to bleaching and salinity fluctuations. In nature, these individuals may not last very long, which may be equally true in the aquarium. The survival of favourable genes which yield stronger individuals is often called "survival of the fittest", a sentence which was first coined by Herbert Spencer (1820-1903) in his book Principles of Biology (1864). Similarly, Charles Darwin, father of the evolution theory, called the selection of stronger individuals over weaker ones "natural selection". In the end, sexual reproduction will yield a diverse population in which the stronger individuals will survive. In terms of coral aquaculture, we might lose a portion of our offspring colonies, which is acceptable and even paramount to obtaining strong blood lines. Maintaining genetically diverse captive populations of many coral species seems the most ideal scenario for the future of coral aquaculture. This holds especially true if such colonies are to be reintroduced to the wild, as part of reef restoration programmes.

Next to maintaining genetic diversity, ageing may be a second major incentive to commence large-scale sexual coral reproduction. It is known that many organisms on the planet age, which may be defined as a decreased functional state in genetic makeup, physiology, morphology and reproduction. This decreases the overall fitness of any organism. There is some evidence which supports the idea that Cnidarians age, including corals^2,3,4. On the other hand, Cnidarians have been found to produce telomerase, an enzyme which inhibits ageing by repairing chromosome ends. This enzyme is also active in tumour cells, which makes these cells immortal. Corals also have effective DNA repair mechanisms⁵, which would also reduce ageing caused by DNA damage. Although it is not yet clear if Cnidarians truly age, sexual reproduction could "reset the clock" for each generation of coral, allowing for long life spans.

Figure 3: Sexual reproduction involves the fertilization of eggs with sperm. Corals have adopted several strategies for successful reproduction, such as releasing gametes in concert on an annual basis. Here, Pocillopora meandrina colonies are releasing eggs and sperm in Hawaii (photograph: Denise Ulrich).

Reproductive strategies

Corals have developed an array of strategies for effective reproduction. In addition to the diverse methods of asexual reproduction, different means of sexual reproduction exist^6,7. These can be categorized based on coral sexuality, and the way gametes are released and fertilized.

- gonochorism/unisexuality

A number of coral families harbours species which are gonochoric, which means males and females exist as separate individuals. His phenomenon is displayed by many animals, including mammals, birds, reptiles, amphibians and fish. The Dendrophyllidae family harbours several genera which utilize this reproductive strategy, such as 2Turbinaria, Tubastrea, Leptopsammia, Heteropsammia, Rhizopsammia, possibly Duncanopsammia, Dendrophyllia and Balanophyllia. These gonochoric animals mainly brood their eggs, which exceptions such as the genus Turbinaria, containing species which release gametes into the water (see broadcasting).

- hermaphroditism/bisexuality

The majority of stony coral species, such as Acropora spp., is hermaphroditic or bisexual. Polyps of such colonies display both active male and female gonads, called testes and ovaries, respectively. These species often release egg/sperm bundles during summer periods, after which the sperm cells are released and fertilize the eggs (see broadcasting). Some species also display self-fertilization, or selfing. This feature occurs amongst some brooding corals. This may occur within the same polyp, or in between polyps of the same colony.

Figure 4: Montipora spp., such as this colony in an artificial lagoon, are hermaphroditic broadcast spawners (photograph: Tim Wijgerde, NAUSICAA, Boulogne-sur-mer, France).

In addition, several species display a unique form of sexuality which involves a transition from one sex to the other, called sequential hermaphroditism. This transition can occur from male to female, called protandry, or from female to male, called protogyny. This phenomenon is often found amongst marine fishes, including anemone fish (Amphiprion and Premnas spp.). The Fungiid corals Fungia repanda and Ctenactis echinata also demonstrate this ability, with the latter species being able to switch back and forth⁸. At any given time, sequential hermaphrodites only have one active gonad type, whereas the other lies dormant and does not produce gametes. For example, a female mushroom coral may have active ovaries and produce/expel oocytes, and have dormant testes at the same time which may become active the following year. Whereas corals may switch sex every season, fish such as pygmy angels may undergo sex change within eight weeks!

Why has (sequential) hermaphroditism evolved? This may be because it is an effective strategy for sexual reproduction, as any two individuals from the same species may be able to fertilize one another. This circumvents the problem of an incidental lack of either males or females in a given population. Second, sequential hermaphroditism allows an individual to produce sperm instead of eggs during times of stress, which is a lot more economical as sperm require much less energy to produce. Eggs have to be loaded with protein and fats, which is undesirable for any organism during times of physiological stress. It has been found that mushroom corals such as Ctenactis echinata reproduce as males when they are small or stressed by sedimentation or bleaching. 

Figure 5: Mushroom corals predominantly exist as solitary polyps, and may grow up to 40 cm (16 inches) in diameter. Species from the Fungiidae family may change sex, with small or stressed individuals typically being male. Sex change is a powerful evolutionary adaptation, allowing corals to maintain high fecundity levels even during periods of stress (photograph: Tim Wijgerde, Rotterdam Zoo, Rotterdam, The Netherlands).

- parthenogenesis

Parthenogenesis (parthenos: virgin, genesis: birth) occurs when egg cells undergo cellular mitosis and start embryonic development without prior fertilization. This yields an individual which is similar to its parent, as no genetic contributions have been made by a male partner (it is not cloning, as genetic recombination still yields a genetically distinct animal). The advantage of this strategy is that female organisms are still able to reproduce in the absence of males. The major downside is that the genetic variation of a given population decreases as a result. This decreases the overall fitness of the population, which means it is less able to adapt to changing conditions. Hereditary defects may also become more apparent. Parthenogenesis seems to be quite uncommon amongst corals, and has been reported for Pocillopora damicornis and Porites sp.^6,9

- broadcasting

Many coral species expel their gametes into the water column annually, during a process called broadcast spawning. This reproductive strategy is common amongst species from the Faviidae, Euphyllidae and Acroporiidae families. Members from the Faviidae and Acroporiidae families, such as Favia, Favites, Acropora and Montipora spp. are usually hermaphroditic, and release egg/sperm bundles into the water through the oral pores of their polyps. Members of the Euphyliidae are predominantly gonochoric, such as Euphyllia ancora and E. divisa. E. glabrescens, the Torch coral, is an exception and has been found to be a hermaphroditic brooder.

Broadcasting species usually expel impressive amounts of gametes, of which only a small fraction yields offspring. The fecundity of these corals is therefore very high under ideal circumstances. Their offspring, in the shape of planula larvae, are an important part of the meroplankton present in the ocean and are consumed by many organisms such as crustaceans and whales. Eventually, a small portion (possibly less than 1%) settles onto a reef which may be hundreds of kilometers away from its location of origin.

"Many coral species expel their gametes into the water column annually, a process called broadcast spawning. This reproductive strategy is common amongst species from the Faviidae, Euphyllidae and Acroporiidae families."

Figure 6: A four day-old Trachyphyllia geoffroyi planula larva. Coral larvae swim by means of beating cilia; these are countless tiny hairs which protrude from epidermal cells. Their swimming speed is quite low; about 2 mm (0.08 inches) per second! Their limited locomotory behaviour allows the larvae to scour the available substrate for a suitable location for settlement. The oral pore always develops at the posterior end, or backside of the larvae, which is the smaller top portion in the picture (photograph: Rachel Jones, London Zoo, London, UK).

After external fertilization of eggs in the water column, which often display positive buoyancy, planula larvae develop after 24 to 48 hours. These are usually significantly smaller (75 - 500 micrometer) compared to larvae which are released by brooding species. For this reason, these larvae have developed ways of feeding themselves during this delicate stage.

Larvae which develop from average-sized eggs (around 0.5 mm) mainly feed on egg yolk, and are called lecithotrophic. Smaller larvae, which develop from smaller eggs depend on external nutritive sources and photosynthesis. In that case, the larvae are considered planktotrophic. 

Coral larvae swim around actively by means of cilia; these are tiny hairs which protrude from the epidermal cells of the larvae. Some species produce larvae which develop oral pores during their planktonic stage, such as several Fungia and Acropora sp. This allows these larvae to ingest plankton and detritus from the water, which provides them with energy. Zooxanthellae, which are symbiotic algae from the genus Symbiodinium, are also ingested in this way. Other species produce larvae which do not develop a mouth until after metamorphosis into a primary polyp, which occurs immediately after larval settlement. An example is the threatened Elkhorn coral from the Caribbean, or Acropora palmata.

"Planula larvae of broadcasting species may spend from several days to several weeks as plankton. This has major consequences for the distribution of species and the recovery of damaged reefs."

Figure 7: A young Trachyphyllia geoffroyi  polyp which died several weeks after settlement. The larvae settled within a groove of a ceramic tile, which is a preferable location for many species¹⁰. Reproduction of this species has been unsuccessful until now, and larvae of this species possibly require infection with zooxanthellae during this stage (photograph: Rachel Jones, London Zoo).

Planula larvae of broadcasting species may spend from several days to several weeks as plankton. This has major consequences for the distribution of species and the recovery of damaged reefs, which may be reseeded as a result of planula dispersion. This long so-called larval competency period allows for large distribution of many coral species.

- brooding

Brooding species expel sperm cells just like broadcasting species, however fertilization of ova occurs internally. Male or hermaphrodite colonies release sperm cells, of which a small proportion finds its way to female or other hermaphrodite specimens of the same species, after which fertilization takes place. Next, the eggs develop into relatively large larvae which are released through the oral pores at sizes between 500 - 2,000 μm (0.5 - 2 mm). In contrast to broadcasters, brooding species produce little eggs and large, well-developed larvae. This strategy is thus based on the principle of "quality instead of quantity". The large larvae are often negatively buoyant, and usually settle within 1 or 2 days. This poses great advantages for the aquaculture of such species, as offspring has far less chances of being skimmed off or being removed by protein skimmers. Examples of brooding species are Pocillopora damicornis, Favia fragum and Tubastrea coccinea.

Transmission of zooxanthellae

Many coral species have formed a symbiotic relationship with unicellular Symbiodinium algae, which provide them with the necessary nutrients for growth and survival. When reproducing, many coral species transfer their zooxanthellae to their offspring through ova. This is very common amongst brooding species, in contrast to broadcasters which often produce aposymbiotic eggs. In nature, exceptions to any rule exist, and this holds true for corals as well. Many species from the genera Montipora are broadcast spawners which transfer zooxanthellae through released eggs. This also goes for Pocillopora meandrina, P. eydouxi and P. verrucosa.

Transfer of zooxanthellae to offspring through ova is called vertical transmission, as this occurs from one generation to the next. This process is typical amongst brooding corals, and has been found for about 15% of all photosynthetic coral species¹¹. When aposymbiotic larvae take up zooxanthellae from the water, this is called horizontal transmission; each generation of offspring therefore has to take up a new batch of symbiotic algae. Both strategies have their (dis)advantages. Vertical transmission ensures higher chances of survival for coral larvae, as they receive vital nutrients from photosynthesis. This only goes for situations where water temperatures do not exceed 30°C (86°F), as high temperatures cause the zooxanthellae to fall apart and release oxygen radicals to the larval tissue^12,13. This leads to significant larvae mortality, and this phenomenon may be the reason why many species do not transfer zooxanthellae to their offspring, circumventing the useful but sometimes precarious symbiosis at early coral life⁶. Another downside of vertical transmission is low flexibility, as the larvae do not get to obtain other zooxanthellae clades, which may be better adapted to high temperatures. This is especially true if larvae end up at new locations where water temperatures are higher on average, which may render them more sensitive to bleaching episodes. Horizontal transmission has this advantage, which may be highly beneficial if larvae drift hundreds of kilometers away to warmer areas. Here, they may take up clade D zooxanthellae, which can be thermally tolerant up to 32°C (90°F). Of course, the major downside here is that these larvae have to rely on other nutritive sources until they acquire zooxanthellae. By feeding on their egg yolk initially, and by consuming plankton and taking up dissolved nutrients such as amino acids and DOC they can survive without Symbiodinium algae.

"Transfer of zooxanthellae to offspring through egg cells is called vertical transmission. Uptake of zooxanthellae from the water column is referred to as horizontal transmission."

Reproduction in the aquarium

The reproductive biology of corals has major consequences for the success of captive sexual reproduction; especially broadcasting species are highly difficult to reproduce in any closed aquarium. In part II, the challenges, possible solutions and future perspectives of captive coral reproduction will be discussed. These challenges involve simulation of environmental cues which stimulate reproduction (such as fluctuations in water temperature), providing ample nutrition and the usage of alternative filtration systems.

Visit www.reefbase.org and www.secore.org for more information about coral reproduction and reef restoration. For a comprehensive list of stony corals and their reproduction methods, the reader is referred to the article of Dana Riddle in Advanced Aquarist's Online Magazine (2008). 

Acknowledgements

The author wishes to thank Dana Riddle for critically evaluating and improving the manuscript.

References:

Wabnitz C., M. Taylor, E. Green and T. Razak, 2003. From ocean to aquarium: The global trade in marine ornamental species, UNEP-WCMC Biodiversity Series No 17, pp 65, ISBN: 92-807-2363-4

Elahi R. and P.J. Edmunds, 2007. Tissue Age Affects Calcification in the Scleractinian Coral Madracis mirabilis, Biol. Bull. 212:20-28

Permata W.D. and M. Hidaka, 2005. Ontogenic changes in the capacity of the coral Pocillopora damicornis to originate branches, Zoological Science 22:1197-1203

Rinkevich B. and Y. Loya, Senescense and dying signals in a reef building coral, 1984. Experientia 42:320-322

Rinkevich B., 2008, personal communication

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

Riddle D., 2008. Feature Article: Coral Reproduction, Part Three: Stony Coral Sexuality, Reproduction Modes, Puberty Size, Sex Ratios and Life Spans, Advanced Aquarist's Online Magazine (www.advancedaquarist.com) 7(9)

Loya Y and K. Sakai, 2008. Bidirectional sex change in mushroom stony corals, Proc. R. Soc. B. 275:2335-2343

Stoddart, J.A., 1983. Asexual production of planulae in the coral Pocillopora darnicornis. Mar Biol 76:279-284

Petersen D., M. Laterveer and H. Schuhmacher, 2005. Innovative substrate tiles to spatially control larval settlement in coral culture, Marine Biology 146:937-942

Weis V., 2008, personal communication

Tchernov D., M.Y. Gorbunov, C. de Vargas, S.N. Yadav, A.J. Milligan, M. Häggblom and P.G. Falkowski, 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals, Prod. Natl. Acad. Scienc. USA 101:13531-13535

Yakovleva I.M., A.H. Baird, H.H. Yamamoto, R. Bhagooli, M. Nonaka, M. Hidaka, 2009. Algal symbionts increase oxidative damage and death in coral larvae at high temperatures, Mar. Ecol. Prog. Ser. 378:105-112