Chapter 7. Asexual Reproduction
Some species of coral-reef Asteroidea are known to exhibit both sexual and asexual reproduction (Yamaguchi, 1975 b). The species known to reproduce asexually are detailed by Emson and Wilkie (1980). Rideout (1978) has shown that asexual reproduction is the chief form of reproduction in the asteroid Linckia multifora at Guam. Achituv and Sher (1991) have suggested that Asterina burtoni reproduces only by asexual reproduction in the Mediterranean Sea. However, the relative roles of sexual and asexual reproduction in the population maintenance of other coral-reef asteroid species have not been studied. It is not known whether asexually reproducing species have a regular alternation of sexual and asexual activity, or if sexual reproduction is strongly reduced or even absent in any of these species.
In asteroids, asexual reproduction involves either the splitting of the disc (fission), or the casting off of arms that regenerate new starfish (autotomy). In some species, autotomised arms need not contain any section of disc or madreporite for their survival (Clark, 1913; Edmondson, 1935). In such species, regeneration of a mouth and basic digestive organs, must occur while the regenerating arm is metabolising stored reserves of energy (Lawrence et al., 1986). A description of the stages of regeneration, following autotomy in Linckia multifora, is provided by Rideout (1978).
The period of regeneration following autotomy, before the regenerated arms are ready for reautotomy, might be prolonged greatly in species larger than Linckia multifora. Autotomy is reduced when individuals are infected with the parasitic gastropod Stylifer as this parasite inhibits autotomy of infected arms. Because the mortality of regenerating individuals is high (Davis, 1967; Rideout, 1978), though not as great as expected by Clark (1913), this inhibition of autotomy results in greater survival of the parasite (Davis, 1967).
An alternation of sexual and asexual activity has been observed in Nepanthia belcheri (Ottesen and Lucas, 1982). Some sexual activity has been recorded in the asexually reproducing species, Ophidiaster robillardi (Yamaguchi and Lucas, 1984). Other species, such as Asterina anomala and Linckia multifora, often remain small and sexually immature through the continuing process of asexual autotomy or fission. Some sexual activity has been noticed in Linckia multifora and Linckia guildingii (Mortensen, 1937, 1938) but the contribution of this as a means of population maintenance may be outweighed by that of autotomy (Rideout, 1978).
Individuals of any species that exhibited signs of recent autotomy or fission were identified, collected and measured. The presence of comets was considered indicative of asexual reproduction by means of autotomy, and recent disc fission, followed by regeneration of more than half the disc, indicative of reproductive binary fission. The frequency of occurrence of asexual products was recorded for each sampling period. Measurements were taken routinely of the number of arms and the length of the longest arm of each individual. Periodically, all arms of asexual specimens were measured and details of obvious regeneration or autotomy were recorded.
In Linckia multifora and Echinaster luzonicus, the mean major radius (mean R mm), mean minor radius (mean r mm) and mean major/minor radius (R/r) were calculated for each sampling period. The variation throughout the study in mean major radius of these species is discussed further in Chapter 8.
Six species of asteroid occurring at Heron Reef exhibited signs of asexual reproduction either by autotomy or binary fission. Specimens of Linckia guildingii, Linckia multifora, Echinaster luzonicus and Ophidiaster robillardi were observed in varying stages of regeneration following arm autotomy. Specimens of Asterina anomala and Coscinasterias calamaria were observed in varying stages of regeneration following binary fission. Autotomous species can regrow a complete individual from the distal half of an arm, with no need for any portion of the disc or madreporite to be included.
The first stage of regeneration in the autotomised arm is called a comet after its characteristic shape. Comets were encountered frequently in these species and most of the individuals collected in this study had recently autotomised at least one arm, with the remaining arms being in various stages of regeneration. Individuals with all arms of equal length were very uncommon. On several occasions, recently autotomised arms were found alongside the parent animal in the field. In large specimens of Echinaster luzonicus, the process of autotomy can proceed very quickly, and if the animals are handled roughly, arms can be autotomised within seconds. If high water quality and a temperature comparable with that which occurs naturally, are not maintained when Linckia multifora and Echinaster luzonicus are kept in aquaria, freshly autotomised arms die.
During the period of study, large changes in mean major radius were observed in both Linckia multifora and Echinaster luzonicus. At times of smaller mean individual size, the frequency of comet stages in the population was generally higher, but this varied between years. In 1978, the number of comet Echinaster luzonicus found in the field corresponded well with periods of lower mean individual size. For example, in May 1978, 29% of individuals were comets, whereas in August 1978, the proportion of comets was only 15%. This declined to about 5% in June 1979, and did not vary greatly over the remainder of the study. In Linckia multifora the proportion of comets in May, August and November 1978 was 32%. This declined to 8% over the following two years. In 1981 and 1982, the proportion of comets increased to 18%.
The difficulty in locating comet stages will have biased these results. Because the frequency of comets and autotomised limbs was difficult to both sample and analyse (and was not studied in detail), variation in the mean major radius (R) and mean major/minor radius (R/r) was considered a more reliable index of the frequency of autotomy.
In both Linckia multifora and Echinaster luzonicus, variation in the mean major radius (R) and mean major / minor radius (R/r) is illustrated in Figures 7.1 and 7.2. The significance of this variation in mean major radius (R) is discussed further in Chapter 8. While specimens of Linckia guildingii and Ophidiaster robillardi that had recently undergone autotomy were observed throughout the study, only Linckia multifora and Echinaster luzonicus were common enough for this variation in mean size to be analysed.
At Heron Reef, Asterina anomala and Coscinasterias calamaria reproduce by binary fission which results in two halves each regrowing to form two complete individuals. In this case a portion of disc containing a madreporite is always present as both species possess several madreporites on the disc.
The remaining species in the Heron Reef asteroid assemblage, while possessing great powers of regeneration, showed no evidence of using autotomy or fission as a form of asexual reproduction. If parts of the body of these species are autotomised, these parts die and the remaining body regenerates the lost limbs.
Asexual reproduction can offset the effects of intense benthic and planktonic larval predation, as well as those caused by the general vicissitudes of planktonic life which include dispersal loss and starvation (see Yamaguchi, 1975 b; Rideout, 1978; Franklin, 1980; Ottesen and Lucas, 1982; Yamaguchi and Lucas, 1984; Olsen, 1987). On coral reefs, benthic predation of larvae and newly settled recruits might be too high for benthic larval development or brooding behaviour (see Menge, 1975; McClary and Mladenov, 1989; McClary, 1990; Bosch, 1989; Bosch and Pearse, 1990; Komatsu et al., 1990) to be a viable survival strategy.
Two modes of reproduction are employed by some asteroids, one mode allowing the species to disperse, the other, the build-up of population numbers once colonisation is established (Yamaguchi and Lucas, 1984). Cameron and Endean (1982) suggested that autotomy is an adaptation to predation and Birkeland et al (1982) observed autotomy in their study of asteroid predatory interactions. A number of tropical and temperate asteroids are known to undergo regular autotomy (Yamaguchi, 1975 b; Rideout, 1978; Emson and Wilkie, 1980; Crump and Barker, 1985; Mladenov et al., 1989; Dubois and Jangoux, 1990).
The size distribution of Linckia multifora and Echinaster luzonicus varied significantly over the study period (see Table 8.1). While the autotomy rate varied within and between years, the frequency of comet stages in the population was also determined by the survival rate of autotomised arms. This seemed to vary considerably from one year to another. Although comet stages of Linckia guildingii and Ophidiaster robillardi were found, there was no obvious temporal variation in their occurrence. The abundance of these species was not sufficient to allow analysis of the change in mean individual size. Although individuals of Asterina anomala and Coscinasterias calamaria were found in varying stages of regeneration, once again, there appeared to be no temporal pattern in the occurrence of asexual stages (compare with Muenchow, 1978; Ottesen and Lucas, 1982). All specimens of Asterina anomala were small and fissiparous and this species appeared to be distinct from Asterina burtoni, at Heron Reef.
At Heron Reef, sexual reproductive effort appears to be very low in Echinaster luzonicus and Linckia guildingii. No sexual activity was recorded in Linckia multifora at all. Small individuals of these three species resulted invariably from autotomy. It would appear that asexual reproduction is the chief means of population maintenance in these three species. Ophidiaster robillardi is less common than either Linckia guildingii, Linckia multifora or Echinaster luzonicus at Heron Reef. On adjacent Wistari Reef, the density of Ophidiaster robillardi in small patches on the reef crest was considerably higher than at Heron Reef. The spatial distributions of Linckia multifora, Ophidiaster robillardi and Echinaster luzonicus were highly clumped. This patchiness in abundance might be a result of local population increases following an initial sexual colonisation (Ottesen and Lucas, 1982; Mladenov and Emson, 1984; 1990; Crump and Barker, 1985; Johnson and Threlfall, 1987). Linckia multifora and Echinaster luzonicus, together with Disasterina abnormalis (which liberates sticky eggs) occurred at the highest local densities recorded during this study.