Of the colonies with gametes present, 57% of Isopora brueggemanni and 68% of Seriatopora hystrix colonies had multiple developmental stages of gametes at any one time, indicating that both species had multiple, overlapping gametogenic cycles. Consequently, the proportions of colonies with different stages summed to more than 100% (Figure 1B-E). Other studies on brooding corals have also reported multiple overlapping gametogenic cycles or continuous planulae release (including four Madracis species from the Caribbean, Acropora palifera from the Great Barrier Reef and Papua New Guinea and Stylophora pistillata, Seriatopora hystrix and Alveopora daedalea from the Red Sea). Overlapping gametogenic cycles and asynchronous planulae release in brooders has been linked to polyp size and water temperature. Brooders with larger polyps are able to hold more planulae and consequently have longer brooding periods and more synchronous planulae release, while yearly temperature cycles have also been shown to regulate planulation in Caribbean brooding corals.
The results from Scott Reef align with other studies on tropical brooders that reported planulae release all year round. The seasonality of planulation in brooding corals varies with location and species, but generally there appears to be a shorter reproductive season at higher latitudes. At high latitude reefs such as Heron Island (23°S) and Rottnest Island (32°S), Pocilloporidae brooders only released planulae in the summer months, with some colonies observed to have up to three cycles of maturing gametes and planulae per season . The same species (Seriatopora hystrix, Pocillopora damicornis and Stylophora pistillata) reproduced all year round near the equator (Palau, 7.5°N). This pattern is likely related to latitudinal and seasonal variations in temperature, light and colony energetics. For example, at Heron Island and Rottnest Island, water temperatures fall well below 20°C in winter, suggesting that winter water temperatures are too cold for reproduction. However, not all brooding corals from high latitude reefs have short reproductive seasons. For example, P. damicornis releases larvae only during the summer months at Heron Island (23°S), but at a similar latitude in Hawaii (24°N), the same species releases all year round. Biological drivers such as competition, may also influence the length and seasonality of reproduction. In the Red Sea, benthic algal cover increases significantly in the winter months, reducing settlement space for coral larvae and thus providing more favourable conditions for reproduction in the summer months when algal cover declines. Globally, there does not appear to be a consistent trend in breeding season and duration of release for brooding corals, and both appear to vary substantially between species. At Scott Reef, S. hystrix and I. brueggemanni had the protracted reproduction generally seen in tropical brooders, but also appeared to have higher output around broadcast spawning times.
S. hystrix and I. brueggemanni had increased proportions of mature gametes and planulation in the mass spawning months, in autumn (March) and spring (October) (Figure 1). Both species had mature eggs, mature testes and planulae in most of the months studied, with the exception of no mature testes in S. hystrix and no planulae in I. brueggemanni in February. Less maturity in February compared to March, as well as both species having fewer colonies with eggs and testes during April compared to other months, indicated that more colonies were reproducing around the March spawning event. There are advantages to timing the release of planulae to the months of mass spawning, including ideal environmental conditions for gamete maturation, larval settlement and survival. More synchronous release of larvae during spawning times may also improve survival due to predator satiation. There are several records of brooders releasing planulae on the night of mass spawning events, however these records come from other locations and refer to different species to those studied here. For example, mass planulae release by the brooding coral Madracis senaria, has previously been reported to coincide with mass broadcast spawning events in the Caribbean. Additionally, in some colonies of Goniastrea aspera in Okinawa, both brooding and spawning behaviour was observed within the same colony around mass spawning times.
The apparent peak in gamete maturation and planulae release around the times of mass spawning at Scott Reef may reflect ancestral responses to the same proximate and ultimate cues influencing mass spawning in corals. An earlier study suggested that broadcast spawning was the ancestral mode of reproduction in corals, and brooding the derived trait, however more recent phylogenetic studies have described a more complex evolutionary pathway, with the most probable path being gonochoric spawning to gonchoric brooding, then to hermaphroditic brooding and finally hermaphroditic spawning. It is also not uncommon for species to exhibit both brooding and spawning modes of reproduction and there are species that exhibit ‘pseudo brooding’ behaviour for a few hours to a few days.
We also recorded some asynchrony in the timing and proportions of colonies with mature testes and colonies with mature eggs. In October, both S. hystrix and I. brueggemanni had fewer colonies with testes compared to eggs, with ~45% of colonies in both species having mature eggs, but only ~20% of I. brueggemanni and ~8% S. hystrix colonies had mature testes. However, in March, higher proportions of eggs and testes appeared to correspond with one another (Figure 1B-E). The onset of oogenesis precedes spermatogenesis by a few months in most corals, but both sexes usually reach maturity simultaneously. This greatly increases the chances of seeing only eggs in samples and is the most likely reason for many early studies recorded only eggs in their samples. Asynchrony in the initial stages of oogenesis and spermatogenesis partially explains the lower proportions of testes in our samples. However, it is interesting that we recorded high proportions of mature eggs in October for S. hystrix and I. brueggemanni with corresponding low proportions of colonies with testes. One possibility is that reproduction may be limited by sperm production. Similar asynchrony was observed in brooding corals in Panama, and the authors suggested that there was little advantage in synchronising sperm release since unfertilised eggs were not wasted (eggs were either reabsorbed or remained viable for later fertilisation).
These data provide insights into the seasons and months of gametogenesis and planulation. The various stages of development within single colonies indicated that multiple gametogenic cycles were occurring in these brooding species. However, further sampling at finer temporal scales would provide the additional information required to determine how many gametogenic cycles are occurring each year, when exactly sperm and planulae are released, and how closely aligned these times are with mass spawning events (e.g. the same night, week or season). These finer scale details have local management implications. For example, anthropogenic increases in sediment concentrations at the times of sperm or planula release can inhibit fertilisation and larval settlement. In coming decades, patterns of coral reproduction will increasingly be influenced by global climate change. It will be critical to determine whether the times for planulation and gametogenesis of brooding corals are shifting with increasing temperature and more frequent and severe disturbance events, and whether there are subsequent implications for coral community structure. Although the cycles of reproduction reported here were not influenced by acute disturbances, the frequency of disturbances is increasing at Scott Reef, as with most reefs around the world. Scott Reef experienced severe bleaching in 1998 and 2016 and moderate bleaching in 2010. Exposure to potentially damaging cyclones also occurred in 2004, 2005, 2007 and 2012. Broadcast spawning corals synchronise the release of their gametes to one or a few nights of the year. Although a highly successful reproductive mode, synchronised spawning also leaves corals more susceptible to acute disturbances around spawning time. At Scott Reef, autumn spawning corals are particularly vulnerable, releasing their gametes in months that have potential exposure to damaging cyclones and the warmest water temperatures for the year. Consequently, a severe disturbance around a spawning event could eliminate a significant proportion of the year’s reproductive output. In contrast, brooding corals release planulae over many months of the year, making them less susceptible to acute disturbances. Provided that brooding corals do not have higher sensitivity to these stressors, they may maintain a high reproductive output and be better placed to re-colonise a reef following a disturbance event. This, in turn, could facilitate an increase in abundance of brooding corals and a shift in community structure.