4.1 Adult G. fascicularis rearing two years ex situ could reproduce sexually
This study found that G. fascicularis reared in a tank for two years spawned and fertilised successfully, indicating that corals could reproduce sexually ex situ. Several environmental signals (such as seasonal temperature, lunar, and diel cycles) have been shown to influence gametogenesis and spawning of corals in the wild (Babcock et al. 1986; Harrison and Wallace 1990; Babcock et al. 1994; Nozawa et al. 2006; Kongjandtre et al. 2010), however, few studies are about coral reproduction ex situ, as a result, the environmental factors that influence reproduction of corals remain unclear. Petersen et al. (2007) reported that broadcast spawners (13 species) and brooders (11 species) in public aquariums mainly reproduced in open systems under natural light conditions. Survey research thought that temperature fluctuation and nature moonlight might be beneficial to enhance reproduction in captivity, but it is not necessary. In addition, they assumed more species might reproduce in public aquariums without being noticed by the staff owing to the lack of recruitment and of experimental design (larval collection). Broadcast coral of four Acropora species (A. hyacinthus, A. tenuis, A. millepora, and A. microclados) spawned for the first time in a fully closed artificial ex situ closed system mesocosm aquarium design that utilised a microprocessor technology to accurately replicate environmental conditions, including photoperiod, seasonal insolation, lunar cycles, and seasonal temperature (Craggs et al. 2017). After that, they completed the life cycle (i.e., production of an F2 generation) of the coral A. millepora in a fully closed artificial ex situ mesocosm (Craggs et al. 2020). This breakthrough has numerous implications for our understanding of reproductive biology in an ex situ environment, but it is still not clear what direct environmental factors are required to trigger spawning. In our study, the system used natural seawater and light; therefore, moonlight may trigger spawning of G. fascicularis. However, further studies should be conducted to determine the factors affecting their reproduction ex situ.
4.2 G. fascicularis larvae quickly acquire zooxanthellae after settlement which improve early survival rate
The zooxanthellae began to appear 9 d after spawning (4 d after settlement) and were not present in the eggs when observed under a stereomicroscope, which indicated that the zooxanthellae of G. fascicularis larvae came from ambient environment. The juveniles of three species (Goniastrea aspera, Platygyra sinensis, and A. millepora) contained zooxanthellae 10 d after settlement (Babcock 1985). Shlesinge and Loya (1991) found that zooxanthellae of Favia favus and P. lamellina appeared 26–30 d and 16–18 d, respectively, after spawning. G. fascicularis that acquired zooxanthellae earlier could acquire nutrition quicker which facilitated their calcification and metamorphosis, thereby improving their early survival rate. The first days or weeks following settlement are characterised by very high rates of mortality, for example, the survival rate of one-month-old primary polyps is approximately 0.21% and 0.25% in F. favus and P. lamellina, respectively (Shlesinge and Loya 1991); larval survival rate of A. muricata and A. valida decrease substantially to around 50% by the first week and to approximately 10% by the second to third week in the settlement aquaria (Nozawa and Harrison 2008). Our study showed the survival rate of G. fascicularis recruits was 81.87% in the first month which was higher than the above studies and may be related to the rapid acquisition of zooxanthellae. In addition, the appearance time of zooxanthellae is not only associated with species but also with the number of zooxanthellae present in the environment. Asymbiotic coral larvae of A. monticulosa in sediment-containing treatments acquired Symbiodinium earlier and had greater Symbiodinium densities when compared to seawater-only treatments (Adams et al. 2009). The combination of an adult coral and sediment resulted in the highest symbiont acquisition rates by A. millepora recruits, which were up to five-fold greater than those in seawater alone (Nitschke et al. 2016). In this study, we used filtered natural seawater, which provided a source of zooxanthellae for rapid acquisition. The appearance time of zooxanthellae in juvenile G. fascicularis is documented here for the first time.
4.3 Competition with algae is a major factor affecting the growth and survival rate ofG. fascicularisrecruits
The mean diameter of G. fascicularis recruits was 4.74 ± 1.12 mm in the first year. Because little is known about the growth rate of the massive corals for one year ex situ, we compared the diameter to the others in situ and found that the growth rate of G. fascicularis recruits was slower than those reported in the literature for other broadcast corals (Table 2). The survival rate of juveniles decreased continuously during the growth process, particularly in the first four months. The survival rate was only 26.55% in the fourth month and 5.60% after one year. The survival rate of A. tenuis juveniles was 59% at 10 months and 56% at 4 months for A. cervicornis (Nakamura et al. 2011; Henry et al. 2019). Compared to the above studies, the survival rate of G. fascicularis in each month was lower in this study.
Table 2
Growth rates of juvenile corals
Species | Mean diameter (mm) | Age | Literature |
Favia favus | 10 | 1 yr | Shlesinge and Loya 1991 |
Platygyra lamellina | 10 | 8 m | Shlesinge and Loya 1991 |
Diploria labyrinthiformis | 3 | 6 m | Chamberland 2017 |
Platygyru sinensis | 3–4 | 8 m | Babcocka and Mundyb 1996 |
Acropora millepora | 5.1 | 9.3 m | Babcocka 1995 |
Acropora solitaryensis | 3.17 ± 0.96 | 3 m | Nozawa et al. 2006 |
Galaxea fascicularis | 4.74 ± 1.12 | 1 yr | This study |
We assume that the slow growth and low survival rate of juveniles might be due to their competition with algae. The main reasons for post-settlement mortality are competition, sedimentation, and predation (Penin et al. 2010, 2011). Among the dead recruits, there were two types: ones with completely removed or heavily damaged skeletons (i.e., “missing recruits’’) who likely faced predation or were dislodged by grazers, and other ones with intact skeletons (i.e., “dead-intact recruits’’) who were probably killed by other factors such as sedimentation, competition, or starvation (Sato 1985; Hunte and Wittenberg 1992). Due to their small size at settlement, predation faced by coral recruits in their benthic life could be overlooked (Penin et al. 2011). In this study, the intact skeletons of dead recruits were observed in the second month, the recruits were placed on a shelf where there were no benthic organisms fixed and no sediment coverage in the pond, and there was sufficient food with natural seawater. Thus, we concluded that competition with algae was the main factor that affected the growth and survival rate of G. fascicularis recruits. Macroalgae can be a dominant space occupier and can inhibit coral recruitment at multiple stages of the lifecycle (Box and Mumby 2007; Ritson-Williams et al. 2010; Craggs et al. 2019; Henry et al. 2019; Liao et al. 2021). Algae may also affect the development and survival of recruits by producing allelopathic substances or by interfering with the microbial community on corals (Rinkevich and Loya 1987; Thacker et al. 1998; Rasher and Hay 2010). Therefore, harmful algae should be timeously removed during juvenile growth.
In conclusion, this study reveals that adult G. fascicularis could sexually reproduce when kept ex situ for two years. The rapid acquisition of zooxanthellae by larvae helpful to improve early survival rate. The mean diameter of G. fascicularis recruits was 4.74 ± 1.12 mm and the survival rate was 5.60% in the first year. We concluded that the slow growth and low survival rate of recruits may be attributed to competition with algae. We recommend that recruits of G. fascicularis be reared 1 month ex situ and then transferred to the field. There are two reasons for this recommendation: firstly, the larvae will have completed metamorphosis and adapted to the ambient environment ex situ for a period of time, and the survival rate can be relatively improved when transplanted into the wild; secondly, the mortality of recruits increase continuously when kept ex situ for an extended period of time, wasting labour and money. Our results suggest that reef rehabilitation methods that aim to harness coral sexual reproduction might benefit from focusing on the rearing of juveniles through early post-settlement mortality bottlenecks.