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Sex change of mushroom corals
Written by Tim Wijgerde   

Israeli and Japanese scientists recently discovered corals can change sex from male to female and back! Studying the coral species Fungia repanda and Ctenactis echinata, they found these corals can change sex on an annual basis.

Scientists from the Tel Aviv University (Prof. Dr. Yossi Loya) , Israel and the University of the Ryukyus (Dr. Kazuhiko Sakai), Japan, found that the stony coral species Fungia repanda and Ctenactis echinata are able to change sex regularly. It has been known for years that animals change sex from male to female, or back. Coral fish, such as pygmy angels for example, are able to do this.

Being hermaphroditic can have great advantages. It allows a species to reproduce in the absence of either males or females. Being a sequential hermaphrodite, that is being able to switch from male to female, or vice versa, also has these advantages. Next to animals,  many plants are able to switch sex as well.

The experiment

To study the reproductive behaviour of Fungiid corals, the scientists collected 10-20 specimens of several species at Sesoko, Okinawa, Japan. This site is inhabited by tens of thousands of corals! They spawn after the June and August full moon, just after dusk. This is similar to Caribbean corals, which spawn just after the August full moon (such as Acropora palmata). They were at first interested in the modes reproduction of these Fungiid corals; were they either male/female (this is called gonochoristic), or were these corals both male and female (this is called hermaphroditic)? They were very surprised when they suddenly discovered in 2006 that these corals could actually change sex! They were able to change from male to female, which is called protandry, and back from female to male, which is called protogyny. Organisms which change sex during their life are called sequential hermaphrodites, and the process itself thus is called sequential hermaphroditism. This ability has also been found in echinoderms (such as urchins and sea stars), crustaceans, mollusks and polychaete worms (such as bristle worms).

For their research they placed several specimens in five lab aquaria of 2,000 l (500 gallons) each, close to the shore. This setup was connected to the sea, thereby ensuring water quality. The collected coral specimens were very large; Fungia repanda specimens were 85 - 380 mm in diameter, and Ctenactis echinata specimens were 125 - 385 mm in length (figure 1).

Experimental setup

Figure 1: Experimental  setup. Each tagged coral was placed in an individual 40 x 20 x 20 cm aquarium, all of which were then placed in large running seawater containers. (a) Fungia repanda; scale bar is 15 cm. (b) Ctenactis echinata; scale bar is 15 cm. (Loya and  Sakai, P roc. R. Soc. B, 2008).

 Each sampled coral was tagged individually with a numeric plastic tag attached to it by a nylon fishing cord inserted through a thin hole.  This  was drilled at the edge of the coral skeleton with a portable dental drill. No adverse effects on the corals were observed due to the tagging procedures. In the laboratory, they measured the length and width of each coral to the nearest 0.1 mm. The wet weight of each coral was weighed to the nearest 0.1 g, after removing excess moisture. After two weeks of acclimatization in the large running seawater containers, each coral was placed in an individual 40 x 20 x 20 cm aquarium (figure 1), all of which were then placed in the large containers (figure 2).

They started to observe the corals from July 3rd 2004, during and after the full moon. The corals were studied for eight consecutive nights, during which they closed the supply of fresh sea water, to avoid any water connections between the aquaria. When the corals spawned, they noted the sex of each coral by looking at their released gametes under the microscope. In the morning, the water supply was activated again. After these experiments, they put the corals back into the ocean. They repeated this study in 2006 and 2007. The coral tags allowed the scientists to use the same specimens every year, and they always started in June; two weeks before their annual spawning. This allowed the corals to acclimatize to the aquarium setup, making sure the corals would still spawn in 'captivity'. To determine the reproductive state of the corals, they collected five large specimens of each species from January 2007 to October 2007 for histological studies.

Spawnings

In 2004, most individuals of F. repanda and C. echinata spawned five nights after the full moon of July and August, for three consecutive nights (figure 2). The corals started spawning at around 22.00, and continued throughout the night, with different specimens spawning at different hours until the next morning. Some specimens spawned six and seven nights after the full moon, a few on all the three nights, and a few specimens did not spawn at all. In August 2006, spawning again occurred five to seven nights after the full moon at precisely the same time as in 2004. Of the F. repanda breeding population, 28%  had changed sex from male to female, and among the C. echinata breeding corals, 55%  had changed sex (from male to female, and from female to male).

F. repanda & C. echinata

Figure 2: Fungiid coral species and gamete release in aquaria. (a) Fungia repanda; scale bar 2.5 cm and (b) C. echinata; scale bar 1.5 cm. (c) Male F. repanda shedding spermatozoa through the mouth that remained suspended in the water; scale bar 3.5 cm. (d) Female C. echinata expelling eggs through the mouth. The eggs were negatively buoyant and settled on the aquarium floor; scale bar 3.5 cm. (e) Female and male corals spawning in captivity (non-reproductive; NR) scale bar 10 cm. (f)   A female during reproduction (upper left), a male during reproduction (upper right and lower left aquaria) and a non-reproducing coral (lower right); scale bar 5.0 cm (Loya and  Sakai, P roc. R. Soc. B, 2008).

In July 2007, five to seven nights after the full moon of June 30th, most individuals of C. echinata spawned. 80% of those from the original 2006 population had changed sex, out of which 27% changed to the sex recorded in 2004! This means this species was able to change sex into both directions, never before observed in corals!

The fact that corals are also able to do this, again underscores how complex life traits have evolved very early in our planet's evolution. We recently reported that scientists found immune systems in corals, and that they are able to merge together to form chimaeras. Again, we see that sex change and hermaphroditism have already developed in corals; animals which have evolved over 200 million years ago!

Why do corals change sex?

Sex change in corals is very interesting, and it must have a purpose. Bidirectional sex change has also been reported in a variety of plants, which sometimes become male during periods of poor environmental conditions. These conditions can range from  low soil fertility to extreme temperatures. When conditions improve, they become female again. This is because being female uses up more energy; producing egg cells (ova) can only be done when sufficient energy is available. Egg cells are full of yolk, which contains a lot of protein and fat. If organisms are weakened, producing sperm is a better alternative.

These Fungiid corals could also be changing sex due to reasons such as bleaching, disease or sedimentation. When these corals recover, they might turn female again. Indeed, the researchers found that smaller corals are male, whereas larger (and possibly healthier) corals are mostly female! Over 90% of the largest C. echinata individuals (above 1800 g!) were observed to be females, while the smallest reproducing individuals (300–700 g) were all males.

When these corals got larger, their gonads (sex organs) also increased in size. The larger the coral, the more energy was invested into reproduction. Other scientists also reported that small Fungia corals (Fungia scutaria from the Red Sea) were mostly male, whereas very large individuals were all female.

This shows that corals have uniquely adapted to the harsh conditions in the oceans. Even when Fungiid corals have little energy to reproduce, they still try to do so as males.

References:

Yossi Loya and Kazuhiko Sakai, Bidirectional sex change in mushroom stony corals, P roc. R. Soc. B (2008) 275, 2335–2343, Copyright the Royal Society 2008