Reproductive characteristics and gamete development of the soft coral Sclerophytum cf. heterospiculatum in Okinawa Island,Japan

Sexual reproduction data are important to understand how organisms can replenish their populations and proliferate on coral reefs. Despite the importance of such data, the reproductive characteristics of most soft coral species are still unknown. Here, we examined the reproductive strategies of a species from the often-dominant genus Sclerophytum in a coral reef on subtropical Okinawa Island, Japan. DNA barcoding and histological examinations of the tissues were conducted to confirm colony conspecificity and identify reproductive characteristics, respectively, between March 2020 and March 2021. Results indicated that the studied species, identified as Sclerophytum cf. heterospiculatum, exhibits gonochorism with longer oogenesis and shorter spermatogenesis. Female colonies produced immature oocytes throughout the year, with mature oocytes observed from late July to early September, and thus, extended spawning is likely characteristic of this species. In male colonies, spermatogenesis took place over ~5 months, with spermaries present from April through August. Mature spermaries were noted beginning in July and the inferred peak of sperm release was between late August and early September, which suggests that spermatogenesis duration was ~5 months. The largest mean oocyte and spermary sizes (628.45 ± 61.36 and 240.04 ± 49.49 μm, respectively) were both recorded in August. Gamete spawning presumably occurred during the summer season, which suggests seasonality in reproduction as influenced by changes in seawater temperature. However, the proximate cue for exact dates of spawning could be the lunar period because the inferred release of spawning materials seemed to occur between full moon and last-quarter moon phases in both the months of August and September. The results of this study represent the first detailed report of reproductive characteristics of the genus Sclerophytum in Japan.     

Biannual coral spawning decreases at higher latitudes on Western Australian reefs

Seasonal differences in the timing of multi-specific coral spawning between the east and west coasts of Australia may be the result of a genetic legacy or of adaptation to local conditions. Using estimates of the proportions of coral species that spawned in spring and autumn at Ashmore Reef (12°S) and Ningaloo Reef (23°S) in Western Australia, in combination with findings of previous surveys, I examined whether reproductive seasonality varied with latitude. A consistently high proportion of species spawned during the main reproductive season in autumn regardless of latitude. However, there was a clear decrease in the proportion of species spawning in spring, from an average of 49 % at Ashmore Reef (12°S) to 7 % at Ningaloo Reef (23°S). The results of this study suggest that seasonality of coral reproduction in Western Australia reflects environmental gradients and natural selection rather than an inherited genetic legacy.     

Hormones and reproduction in scleractinian corals

Most broadcast spawning scleractinian corals synchronously release gametes during a brief annual spawning period. In southern Taiwan, the mass spawning of scleractinians occurs in lunar mid-March. The exact cues triggering this annual phenomenon remain unclear. A scleractinian coral, Euphyllia ancora has been selected as a model for the hormones and reproduction studies. Testosterone (T) and estradiol (E2) in free and glucuronided forms were identified and consistently detected in coral polyps throughout the year. Peak levels of free E2, glucuronided E2 and T were obtained in the coral tissue just prior to spawning. The presence of specific aromatase activity was demonstrated in coral tissue. Higher concentrations of free E2 than glucuronided E2 were detected in the coral tissue throughout the year. In contrast, higher levels of glucuronided E2 than free E2 and glucuronided T were found in seawater during mass coral spawning. Furthermore, immunoreactivity and biological activity of immunoreactive gonadotropin-releasing hormone (irGnRH) was detected and quantified in coral tissue. Coral extracts (irGnRH) and mammalian (m)GnRH agonist had a similar dose-dependent effect on luteinizing hormone (LH) release in black porgy fish pituitary cells (in vitro). Peak levels of irGnRH were detected during the spawning period. In in vivo experiments, mGnRH agonist time- and dose-dependently stimulated aromatase activity, as well as the levels of T and E2 in free and glucuronided forms in coral. In conclusion, our data suggest that irGnRH and glucuronided E2 may play important roles in the control of reproduction and mass spawning in corals.     

Mass spawning of corals on a high latitude coral reef

Evidence is presented that at least 60% of the 184 species of scleractinian corals found on reefs surrounding the Houtman Abrolhos Islands (Western Australia) participate in a late summer mass spawning. These populations are thus reproductively active, despite most species being at the extreme southern limit of their latitudinal range (28° 29°S). In the present study, coral mass spawning occurred in the same month on both temperate (Houtman-Abrolhos) and tropical (Ningaloo) reefs of Western Australia, despite more than two months difference in the timing of seasonal temperture minima between the two regions. This concurrence in the month of spawning suggests that temperature does not operate as a simple direct proximate cue for seasonal spawning synchrony in these populations. Seasonal variation in photoperiod may provide a similar and more reliable signal in the two regions, and thus might be more likely to synchronize the seasonal reproductive rhythms of these corals. Also there is overlap in the nights of mass spawning on the Houtman Abrolhos and tropical reefs of Western Australia, despite significant differences in tidal phase and amplitude between the two regions. This indicates that tidal cycle does not synchronize with the night(s) of spawning on these reefs. Spawning is more likely to be synchronised by lunar cycles. The co-occurrence of the mass spawning with spring tides in Houtman Abrolhos coral populations may be evidence of a genetic legacy inherited from northern, tropical ancestors. Micro-tidal regimes in the Houtman Abrolhos region may have exerted insufficient selective pressure to counteract this legacy.     

Coral reproduction in the world��s warmest reefs: southern Persian Gulf (Dubai, United Arab Emirates)

Despite extensive research on coral reproduction from numerous geographic locations, there remains limited knowledge within the Persian Gulf. Given that corals in the Persian Gulf exist in one of the most stressful environments for reef corals, with annual variations in sea surface temperature (SST) of 12°C and maximum summer mean SSTs of 36°C, understanding coral reproductive biology in the Gulf may provide clues as to how corals may cope with global warming. In this study, we examined six locally common coral species on two shallow reef sites in Dubai, United Arab Emirates (UAE), in 2008 and 2009 to investigate the patterns of reproduction, in particular the timing and synchrony of spawning. In total, 71% colonies in April 2008 and 63% colonies in April 2009 contained mature oocytes. However, the presence of mature gametes in May indicated that spawning was potentially split between April and May in all species. These results demonstrate that coral reproduction patterns within this region are highly seasonal and that multi-species spawning synchrony is highly probable. Acropora downingi, Cyphastrea microphthalma and Platygyra daedalea were all hermaphroditic broadcast spawners with a single annual gametogenic cycle. Furthermore, fecundity and mature oocyte sizes were comparable to those in other regions. We conclude that the reproductive biology of corals in the southern Persian Gulf is similar to other regions, indicating that these species have adapted to the extreme environmental conditions in the southern Persian Gulf.     

Larval development of certain gamete-spawning scleractinian corals

Embryogenesis and larval development were documented in 19 species of hermatypic scleractinians which release gametes during the summer coral spawning season on the Great Barrier Reef. Cleavage of fertilized eggs began approximately 2 h after spawning in all species, and gave rise to blastulae after 7–10 h. Endoderm formation in Platygyra sinensis was by invagination, and this appeared to occur in all species studied. All species observed at 36 h after spawing were mobile and full mobility was reached by 48 h. Settlement of planulae placed in aquaria occurred between 4 and 7 days after fertilization. These results suggest that larval corals produced by most gamete-releasing coral species are likely to be dispersed away from the parent reef.     

Gonadal development and spawning of female ocean whitefish, Caulolatilus princeps (Pisces: Branchiostegidae) in the Bay of La Paz, B.C.S., Mexico

The developmental stages of the gonads and the spawning season of the ocean whitefish, Caulolatilus princeps , were determined. Gonad maturation is annual, and the spawning season is prolonged, from late autumn to early spring. From November to March, around 80% of the females were in an advanced mode of gonadal development, and in April most gonads were spent. From May to October the gonads were at rest and preparing for the next spawning season.
The gonadosomatic index describes the reproductive activity of the species adequately.     

Reproductive patterns in three species of large coral reef sponges

The type and frequency of reproduction of three common sponge species was monitored histologically and by direct field observations of spawning events over 2 successive years at the reefs of Curaçao. Ircinia strobilina showed year round reproductive activity by the production of spermatic cysts in varying intensities in a major part of the population. Production of oocytes and larvae were only observed in the period from September through April, indicating an actual breeding season of 8 months a year. The sexes in this viviparous sponge seem to be separate, but protandry cannot be ruled out. Less than 10% of the sponge tissue was found to consist of reproductive elements. Neofibularia nolitangere is a gonochoristic oviparous sponge with a short annual breeding season of 2 months, in which two successive, highly predictable, short spawning periods occurred synchronously for the whole population. Up to half of the sponge tissue was transformed to reproductive elements. Agelas clathrodes showed low reproductive activity. Field observation suggests that this sponge is an oviparous hermaphrodite, probably annually releasing male and female gametes synchronously in a varying number of individuals of its population during a short breeding period.The variation in reproductive patterns in this small group of large massive coral reef sponges spans a range similar to that found in the morphologically highly variable group of stony corals and illustrates their ecological differentiation on the reef.     

Annual cycles of solar insolation predict spawning times of Caribbean corals

Seasonal increases in sea surface temperature (SST) have long been considered the trigger for mass spawning events in reef corals. We critically examined the relationship between SST and the spawning activity of broadcasting corals in the tropical western Atlantic (Caribbean). This meta-analysis examined 12 species of broadcasting corals at 25 sites spanning 22 degrees of latitude (10°–32° N) from Venezuela to Bermuda in the Atlantic Ocean from 1986 to 2004. Sigmoidal logit regression models were used to examine the relationship between the release of reef-coral gametes and the environmental variables SST and solar insolation defined as (1) the cumulative response 7–10 months prior to spawning (integral); (2) the rate of change at the time of spawning (derivative); and (3) the average for the month of spawning. The Quasi–Newton method was used to estimate the maximum likelihood of the response function. We demonstrate that the recent history and rate of change in temperature correlate poorly with the timing of spawning, while the average temperature during the month of spawning was significant (with all corals releasing gametes 28–30 °C, except Montastraea annularis , which released gametes at 27–30 °C). In contrast, the rate of change and the cumulative response of solar insolation cycles was a better predictor of gamete release, but solar insolation intensity at the time of spawning was not. These models have important implications for predicting coral reproductive cycles in all oceans, and for examining other marine phototrophic systems beyond corals.     

New insights into patterns of coral spawning on Western Australian reefs

On reefs around Australia, coral mass spawning typically occurs during the austral spring (October/November) on the east coast, and during autumn (March/April) on the west coast. However, to investigate the incidence of a secondary spawning event in spring on the west coast, the reproductive state of corals was assessed on two reefs. The results indicated that of the 29 species of Acropora investigated, multiple colonies of 11 species spawned in late spring or in early summer, in contrast to previous reports of spawning during autumn. Additionally, of four species that were followed through time at one reef, two spawned in both spring and autumn, however, individual colonies had only one gametogenic cycle. Within a single site, conspecific colonies were reproductively isolated and may not interbreed, potentially representing the initial stage of sympatric speciation in these populations.     

Cryopreservation of sperm from the coral Acropora humilis

Corals are sensitive to minute changes in their environments, and their continued existence is substantially threatened by the increasing number of destructive anthropogenic activities and unprecedented rates of climate change. Although cryopreservation has been successfully to preserve mammalian gametes for decades, coral cryopreservation was attempted for the first time less than 15 years ago, and freezing protocols exist for only a handful of coral species. The present study developed a cryopreservation protocol for the sperm of the common Indo-Pacific reef-builder Acropora humilis. Colonies of reefs of Sattahip Bay, Chonburi Province, Thailand were collected from 3 m depth with a mesh net during a spawning event. Immediately after collection, the sperm were isolated and subjected to a two-step freezing method featuring DMSO, polyethylene glycol, or methanol as the cryoprotectant. Viability and motility were assessed via a bioluminescence technique and a “computer-assisted semen analysis, and it was found that a 15-min equilibration with 2 M DMSO followed by cooling at 41.7 °C was the optimum cryopreservation protocol for A. humilis sperm. The post-thaw sperm achieved 45% fertilization success, and 35% of the fertilized eggs developed into blastopore larvae. The present optimized protocol can therefore facilitate the preservation of sperm for future propagation efforts of this species and provide an experimental platform for optimizing cryopreservation protocols for gametes of other scleractinian coral species.     

Sexual reproduction of Acropora reef corals at Moorea, French Polynesia

Little information is available on reproductive processes among corals in isolated central Pacific reef regions, including French Polynesia. This study examined the timing and mode of sexual reproduction for Acropora reef corals at Moorea. Spawning was observed and/or inferred in 110 Acropora colonies, representing 12 species, following full moon periods in September through November 2002. Gamete release was observed and inferred in four species of Acropora between 9 and 13 nights after the full moon (nAFM) in September 2002. Twelve Acropora spp. spawned gametes between 5 and 10 nAFM in October 2002, with six species spawning 7 nAFM and four species spawning 9 nAFM. In November 2002, spawning of egg and sperm bundles was observed and inferred in 27 colonies of Acropora austera, 6 nAFM. These are the first detailed records of spawning by Acropora corals in French Polynesia.     

Biogeochemical responses following coral mass spawning on the Great Barrier Reef: pelagic–benthic coupling

This study quantified how the pulse of organic matter from the release of coral gametes triggered a chain of pelagic and benthic processes during an annual mass spawning event on the Australian Great Barrier Reef. Particulate organic matter (POM) concentrations in reef waters increased by threefold to 11-fold the day after spawning and resulted in a stimulation of pelagic oxygen consumption rates that lasted for at least 1 week. Water column microbial communities degraded the organic carbon of gametes of the broadcast-spawning coral Acropora millepora at a rate of >15% h⁻¹, which is about three times faster than the degradation rate measured for larvae of the brooding coral Stylophora pistillata. Stable isotope signatures of POM in the water column reflected the fast transfer of organic matter from coral gametes into higher levels of the food chain, and the amount of POM reaching the seafloor immediately increased after coral spawning and then tailed-off in the next 2 weeks. Short-lasting phytoplankton blooms developed within a few days after the spawning event, indicating a prompt recycling of nutrients released through the degradation of spawning products. These data show the profound effects of coral mass spawning on the reef community and demonstrate the tight recycling of nutrients in this oligotrophic ecosystem.     

Reproductive biology of Hemiramphus brasiliensis and H. balao (hemiramphidae): maturation,spawning frequency,and fecundity

Analyses of life-history data show that both the size-specific batch fecundities and the age-specific spawning frequencies differ for two halfbeak species, Hemiramphus brasiliensis, the ballyhoo, and H. balao, the balao. Halfbeak ages were determined from sectioned otoliths; histological data was used to describe oocyte development and estimate spawning frequency; and batch fecundity was measured from counts of whole oocytes in final maturation. Hemiramphus brasiliensis lived longer (4 versus 2 years) and had a higher survival rate (14.9% versus 7.5% annually) than H. balao did. Of the two species the larger and longer-lived congener, H. brasiliensis, reached sexual maturity at a larger size (fork length 198 versus 160 mm). The spawning period of age-0 females was strongly related to season, whereas spawning by older females occurred throughout the year. Reproduction by both species peaked during late spring or early summer, and all mature females were spawning daily during April (H. brasiliensis) or June (H. balao). This is the first demonstration of iteroparity for the family Hemiramphidae. H. brasiliensis had a lower batch fecundity (about 1164 versus 3743 hydrated oocytes for a 100-g female) than H. balao did. Such low batch fecundities are typical of the order Beloniformes, but quite different from those of other fishes that live in association with coral reef habitats. H. balao's higher batch fecundity is consistent with the life-history theory that predicts higher numbers of eggs for shorter-lived species; this is possible because H. balao produces smaller hydrated oocytes than H. brasiliensis (modal diameter about 1.6 versus 2.4 mm). The high spawning frequency of Hemiramphus species compensates for their low batch fecundity. The annual fecundity of both species is similar to that of other reef fish species, after adjusting for body size and spawning frequency. The lifetime fecundity of H. balao was very similar to that of H. brasiliensis, after accounting for the differences in survival for each species. This suggests a fine tuning of different reproductive traits over the entire life cycle that results in roughly equivalent lifetime fecundity for both species.     

Estrone and estradiol-17 beta concentration in tissue of the scleractinian coral, Montipora verrucosa

Spawnings of scleractinian corals are affected by light, temperature, and other environmental cues, but no studies elucidate physiological mechanisms that regulate coral gametogenesis. We hypothesized that estrogens may act as bioregulators of coral reproduction. Estrone (E1) and estradiol-17 beta (E2) concentrations were measured in homogenates of tissue and skeleton from M. verrucosa. Tissue samples were collected monthly throughout the year, and more frequently in July and August around spawning. Steroids were extracted with diethyl ether, purified via celite chromatography and assayed with radioimmunoassay. Non-specific binding in coral tissue varied with sample weight and was elevated relative to standards. Monthly mean E1 ranged from 20-70 ng E1 g ash-free dry weight (AFDW)-1, with highest values in April. Smaller asynchronous peaks occurred in early July, prior to spawning. Monthly mean E2 ranged from 8-25 ng E2 g AFDW-1, with highest values in February and March. Peaks in E2 preceded peaks in E1, indicating metabolism of a pool of estrogen. E1 was positively correlated with protein concentration, which is consistent with a bioregulatory role of estrogens. Estrogen peaks in spring and prior to the July spawn corroborate our hypothesis that estrogens regulate coral gametogenesis and spawning.     

Synchronous reproduction of corals in the Red Sea

Multi-species synchronous spawning was first described on reefs off the east and west coast of Australia. In contrast, locally abundant species in the northern Red Sea and the central Pacific have little overlap in the time of reproduction. Consequently, the idea developed that high levels of spawning synchrony both within and among species was largely confined to Australian reefs. Here, we show that gamete maturity in colonies of the genus Acropora was highly synchronous in the Red Sea. In early April 2008, at two locations separated by 300 km, 13 of 24 species sampled had mature colonies, and a further 9 species had immature colonies. In late April–early May 2008, all colonies sampled had no oocytes, indicating colonies had spawned a few days after the full moon of 20 April 2008. Similarly, in 2009, 99% of colonies from 17 species at Hurghada were mature in late April, and all were empty in early May. Spawn slicks suggested many of these colonies had released gametes three night prior to the full moon on 8 May 2009. This level of synchrony in gamete maturity is among the highest ever recorded and similar to that typically recorded in Acropora assemblages on Australian reefs. While further work is required to document the night of gamete release, these data strongly suggest that high levels of spawning synchrony are a regular feature of these Red Sea coral assemblages and that multi-species spawning occurs on or around the full moon in April and/or May.     

Broadcast Spawning by Pocillopora Species on the Great Barrier Reef

The coral genus Pocillopora is one of the few to include some species that broadcast spawn gametes and some species that brood larvae, although reports of reproductive mode and timing vary within and among species across their range. Notably, the ubiquitous Pocillopora damicornis has been described as both a brooder and spawner, although evidence of broadcast spawning is rare. Here, we report observations of broadcast-spawning in four species of Pocillopora on the Great Barrier Reef (GBR), including P. damicornis. All species spawned predictably during the early morning, two days following the full moon, and spawning was observed in multiple months over the summer period (November to February). Eggs and sperm were free-spawned concurrently. Eggs were negatively buoyant and contained Symbiodinium. This newfound knowledge on the mode, timing and regularity of broadcast spawning in Pocillopora spp. on the GBR brings us one step closer to elucidating the complex reproductive ecology of these species.     

Spawning synchrony in Arenicola marina: evidence for sex pheromonal control

Chemical communication systems controlling reproductive behaviour have been shown in a number of marine polychaetes. This study investigated the use of sex pheromones to coordinate spawning behaviour in gravid lugworms (Arenicola marina). Lugworms typically reproduce in the autumn, during low water of spring tides, and often exhibit epidemic spawning. Females release gametes within the burrow whereas males deposit spermatozoa on to the beach surface. The incoming tide dilutes the spermatozoa and transports them to the females'' burrows. Sperm is diluted rapidly and sperm concentrations fall below the minimum required for fertilization within a few minutes. The present investigation establishes the existence of chemical signals synchronizing spawning for the first time in an iteroparous polychaete. The process can be divided into two steps, the induction of gamete release by waterborne chemical cues and burrow irrigation behaviour in females: burrow irrigation representing the means by which spermatozoa are carried to the eggs. In both sexes, the release of gametes can be induced by exposure to sea water into which other individuals had previously spawned. Males also respond to odour compounds from other males. The overall effect of the chemical signals results in synchronized, mass spawning of a population.     

Genetic, spatial, and temporal components of precise spawning synchrony in reef building corals of the Montastraea annularis species complex

When organisms release gametes into the sea, synchrony must be precise to increase fertilization and decrease hybridization. We tagged and genotyped over 400 spawning corals from the three species in the Montastraea annularis species complex. We report on the influence of species, individuals, and genotypes on timing of spawning from 2002 through 2009. During their annual spawning event M. franksi spawns on average 2 h after sunset, whereas M. annularis and M. faveolata spawn 3.5 h after sunset. Only M. franksi and M. annularis have compatible gametes. Individual colonies of the same genotype spawn at approximately the same time after sunset within and across years (within minutes), but different genotypes have significantly different spawning times. Neighboring colonies, regardless of genotype, spawn more synchronously than individuals spaced further apart. At a given distance, clone-mates spawn more synchronously than nonclone-mates. A transplant experiment indicates a genetic and environmental influence on spawn time. There is strong, but not absolute, concordance between spawn time, morphology, and genetics. Tight precision in spawning is achieved via a combination of external cues, genetic precision, and perhaps conspecific signaling. These mechanisms are likely to influence reproductive success and reproductive isolation in a density-dependent manner.