Elevated Temperature Alters the Lunar Timing of Planulation in the Brooding Coral Pocillopora damicornis

Reproductive timing in corals is associated with environmental variables including temperature, lunar periodicity, and seasonality. Although it is clear that these variables are interrelated, it remains unknown if one variable in particular acts as the proximate signaler for gamete and or larval release. Furthermore, in an era of global warming, the degree to which increases in ocean temperatures will disrupt normal reproductive patterns in corals remains unknown. Pocillopora damicornis, a brooding coral widely distributed in the Indo-Pacific, has been the subject of multiple reproductive ecology studies that show correlations between temperature, lunar periodicity, and reproductive timing. However, to date, no study has empirically measured changes in reproductive timing associated with increased seawater temperature. In this study, the effect of increased seawater temperature on the timing of planula release was examined during the lunar cycles of March and June 2012. Twelve brooding corals were removed from Hobihu reef in Nanwan Bay, southern Taiwan and placed in 23 and 28°C controlled temperature treatment tanks. For both seasons, the timing of planulation was found to be plastic, with the high temperature treatment resulting in significantly earlier peaks of planula release compared to the low temperature treatment. This suggests that temperature alone can influence the timing of larval release in Pocillopora damicornis in Nanwan Bay. Therefore, it is expected that continued increases in ocean temperature will result in earlier timing of reproductive events in corals, which may lead to either variations in reproductive success or phenotypic acclimatization.     

Geographical variation in reproductive biology is obscured by the species problem: a new record of brooding in Porites cylindrica,or misidentification?

Little is known about the reproductive biology of corals from the Philippines, despite this archipelago being at the center of coral reef biodiversity. Here, we report on the reproductive biology of a branching poritid species provisionally identified as Porites cf. cylindrica in the Bolinao‐Anda reef complex (BARC), northwestern Philippines. Histological examination and ex situ planulation observations reveal P.cf. cylindrica colonies to be gonochoric brooders that release actively swimming zooxanthellate larvae. Planulation appeared to occur throughout the year and there was significant lunar periodicity in planular release. The mean peak of release occurred from the 25th to 29th lunar day or just before the new moon, while peak in diel timing in planulation occurred during daytime between 08:00–11:00 h. Elsewhere in the Pacific, Porites cylindrica colonies are reported to broadcast spawn. If our species identification is correct, then this is the first report of brooding in P. cylindrica. Although there are no apparent morphological differences between the coral in this study and P. cylindrica reported from other sites, an alternative explanation for our findings is that our provisionally identified Porites cf. cylindrica is a different species. If so, our findings further highlight how difficulties with species identification in corals can influence our understanding of geographical variation in reproductive biology.     

Circadian clock gene expression in the coral Favia fragum over diel and lunar reproductive cycles

Natural light cycles synchronize behavioral and physiological cycles over varying time periods in both plants and animals. Many scleractinian corals exhibit diel cycles of polyp expansion and contraction entrained by diel sunlight patterns, and monthly cycles of spawning or planulation that correspond to lunar moonlight cycles. The molecular mechanisms for regulating such cycles are poorly understood. In this study, we identified four molecular clock genes (cry1, cry2, clock and cycle) in the scleractinian coral, Favia fragum, and investigated patterns of gene expression hypothesized to be involved in the corals' diel polyp behavior and lunar reproductive cycles. Using quantitative PCR, we measured fluctuations in expression of these clock genes over both diel and monthly spawning timeframes. Additionally, we assayed gene expression and polyp expansion-contraction behavior in experimental corals in normal light:dark (control) or constant dark treatments. Well-defined and reproducible diel patterns in cry1, cry2, and clock expression were observed in both field-collected and the experimental colonies maintained under control light:dark conditions, but no pattern was observed for cycle. Colonies in the control light:dark treatment also displayed diel rhythms of tentacle expansion and contraction. Experimental colonies in the constant dark treatment lost diel patterns in cry1, cry2, and clock expression and displayed a diminished and less synchronous pattern of tentacle expansion and contraction. We observed no pattern in cry1, cry2, clock, or cycle expression correlated with monthly spawning events suggesting these genes are not involved in the entrainment of reproductive cycles to lunar light cycles in F. fragum. Our results suggest a molecular clock mechanism, potentially similar to that in described in fruit flies, exists within F. fragum.     

Gene expression under chronic heat stress in populations of the mustard hill coral (Porites astreoides) from different thermal environments

Recent evidence suggests that corals can acclimatize or adapt to local stress factors through differential regulation of their gene expression. Profiling gene expression in corals from diverse environments can elucidate the physiological processes that may be responsible for maximizing coral fitness in their natural habitat and lead to a better understanding of the coral's capacity to survive the effects of global climate change. In an accompanying paper, we show that Porites astreoides from thermally different reef habitats exhibit distinct physiological responses when exposed to 6 weeks of chronic temperature stress in a common garden experiment. Here, we describe expression profiles obtained from the same corals for a panel of 9 previously reported and 10 novel candidate stress response genes identified in a pilot RNA‐Seq experiment. The strongest expression change was observed in a novel candidate gene potentially involved in calcification, SLC26, a member of the solute carrier family 26 anion exchangers, which was down‐regulated by 92‐fold in bleached corals relative to controls. The most notable signature of divergence between coral populations was constitutive up‐regulation of metabolic genes in corals from the warmer inshore location, including the gluconeogenesis enzymes pyruvate carboxylase and phosphoenolpyruvate carboxykinase and the lipid beta‐oxidation enzyme acyl‐CoA dehydrogenase. Our observations highlight several molecular pathways that were not previously implicated in the coral stress response and suggest that host management of energy budgets might play an adaptive role in holobiont thermotolerance.     

Deepwater broadcast spawning by Montastraea cavernosa, Montastraea franksi, and Diploria strigosa at the Flower Garden Banks, Gulf of Mexico

Broadcast spawning by corals is a tightly synchronized process characterized by co-ordinated gamete release within 30–60 min time windows once per year. In shallow water corals, annual water temperature cycles set the month, lunar periodicity the day, and sunset time the hour of spawning. This tight temporal regulation is critical for achieving high fertilization rates in a pelagic environment. Given the differences in light and temperature that occur with depth and the importance of these parameters in regulating spawn timing, it has been unclear whether deeper coral can respond to the same environmental cues that regulate spawning behaviour in shallower coral. In this report, a remotely operated vehicle was used to monitor coral spawning activity at the Flower Garden Banks at depths from 33 to 45 m. Three species Montastraea cavernosa, Montastraea franksi, and Diploria strigosa were documented spawning within this depth range. All recorded spawning events were within the same temporal windows as shallower conspecifics. These data indicate that deep corals at this location either sense the same environmental parameters, despite local attenuation, or communicate with shallower colonies that can sense such spawning cues.     

Planulation patterns of the brooding coral <Emphasis Type="Italic">Favia</Emphasis> <Emphasis Type="Italic">fragum</Emphasis> (Esper) in Bermuda

Planulation by Favia fragum at the high-latitude reef of Bermuda was examined during July and August of 2004–2007. In 2004 and 2005, observations were extended to June and September; however, planulation only occurred in July and August, when temperatures were increasing toward and during the annual high. Planulation peaked 6–12 days after the new moon, corresponding to the pattern found for F. fragum in the Caribbean. Mean monthly fecundity was also similar to that found in the Caribbean; however, annual and monthly fecundity were variable, being lowest in July 2005, which coincided with lowest mean SST. These results indicate that although fecundity and lunar timing of planulation by F. fragum are not affected by latitude, reproductive seasonality may be shorter at high-latitude reefs. Understanding reproductive events at latitudinal extremes gives insight to environmental controls on coral reproduction, which will aid in future management and restoration efforts.     

Siderastrea siderea spawning and oocyte resorption at high latitude

Abstract

At high latitudes (>25°), sexual reproduction and the maintenance of coral populations can be impaired by marginal environmental conditions. However, little is known about sexual reproduction of many coral species at high latitude on the northern-most extension of the Florida Reef Tract. This study aimed to histologically characterize the reproductive ecology of Siderastrea siderea, near Fort Lauderdale, Florida (26°N). Tissue samples of S. siderea were collected semi-monthly to multi-weekly from August to November in 2007 and 2008. Spawning was inferred from gametogenesis and oocyte resorption was observed in detail. Environmental variables including temperature and lunar cycle were examined for relationship with potential spawning times. Based on the histological evidence, we infer that spawning likely occurred primarily in October. Gametogenesis in this species is likely mediated by seasonal temperature variation, whereas lunar cycle could act as finer scale environmental cue for coordination of spawning. Our findings highlight that S. siderea spawning occurs later in the year compared to other populations of this species throughout the Caribbean and to other coral species near Fort Lauderdale. For the first time, oocyte resorption stages are described and constitute a baseline for future projects that aim to understand this process in corals.     

Associations between climate stress and coral reef diversity in the western Indian Ocean

Climatic–oceanographic stress and coral reef diversity were mapped in the western Indian Ocean (WIO) in order to determine if there were associations between high diversity coral reefs and regions with low‐to‐moderate climate stress. A multivariate stress model developed to estimate environmental exposure to stress, an empirical index of the coral community's susceptibility to stress, and field data on numbers of fish and corals taxa from 197 WIO sites were overlain to evaluate these associations. Exposure to stress was modeled from satellite data based on nine geophysical–biological oceanographic characteristics known to influence coral bleaching (i.e. temperature, light, and current variables). The environmental stress model and the coral community's susceptibility index were moderately correlated (r=?0.51) with southern and eastern parts of the WIO identified as areas with low environmental stress and coral communities with greater dominance of bleaching stress‐sensitive taxa. Numbers of coral and fish taxa were positive and moderately correlated (r=0.47) but high diversity regions for fish were in the north and west while diversity was highest for corals in central regions from Tanzania to northwestern Madagascar. Combining three and four of these variables into composite maps identified a region from southern Kenya to northern Mozambique across to northern–eastern Madagascar and the Mascarene Islands and the Mozambique–South Africa border as areas where low‐moderate environmental exposure overlaps with moderate‐high taxonomic diversity. In these areas management efforts aimed at maintaining high‐diversity and intact ecosystems are considered least likely to be undermined by climate disturbances in the near term. Reducing additional human disturbances, such as fishing and pollution, in these areas is expected to improve the chances for their persistence. These reefs are considered a high priority for increased local, national, and international management efforts aimed at establishing coral reef refugia for climate change impacts.     

Life‐history traits of Tubastraea coccinea: Reproduction,development, and larval competence

The sun coral Tubastraea coccinea Lesson, 1829 (Dendrophylliidae) is a widely distributed shallow‐water scleractinian that has extended its range to non‐native habitats in recent decades. With its rapid spread, this coral is now one of the main invasive species in Brazil. Its high invasive capability is related to opportunistic characteristics, including several reproductive strategies that have allowed it to disperse rapidly and widely. To better understand the reproductive biology of T. coccinea and aid in developing management strategies for invaded areas, we investigated aspects of its reproductive performance and life cycle, including the effects of colony size, seawater temperature and salinity, and lunar periodicity on offspring production and larval metamorphosis competence. A total of 18,139 offspring were released in different developmental stages, mainly from the larger colonies, which also produced larvae with longer competence periods. The main reproductive peak occurred during the First Quarter and New Moon phases and was highest in water temperatures around 26°C. Together, these results help to explain the rapid expansion of T. coccinea into non‐native habitats such as the Caribbean and southwestern Atlantic, and will inform actions of the recent Brazilian National Plan for the prevention, eradication, control, and monitoring of sun corals.     

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.     

Reproduction and developmental pathways of Red Sea Xeniidae (Octocorallia,Alcyonacea)

This work on Red Sea alcyonaceans describes the reproductive patterns of 21 xeniid species. Gonochorism is the commonest sexual mode but simultaneous hermaphroditism was recorded in 4 species and brooding of planulae was observed in 15 species. The reproductive patterns of Xenia umbellata and Heteroxenia fuscescens were examined. X. umbellata exhibits seasonal spermatogenesis, continuous oogenesis and a 7 month period of planulation each year. H. fuscescens has continuous gametogenesis, and planulation occurs throughout the year, lacking any lunar pattern. The prolonged breeding season of H. fuscescens reflects intrapopulation asynchrony in larval development and subsequent maturation. Xeniids possess structurally similar gonads, but adopt diverse reproductive and developmental pathways.     

Responses of coral‐associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host

This study compared the effect of heat stress on coral‐associated bacterial communities among juveniles of the coral, Acropora tenuis, hosting different Symbiodinium types. In comparison to a control temperature treatment (28 °C), we documented dramatic changes in bacterial associates on juvenile corals harbouring ITS 1 type D Symbiodinium when placed in a high (32 °C) temperature treatment. In particular, there was a marked increase in the number of retrieved Vibrio affiliated sequences, which coincided with a 44% decline in the photochemical efficiency of the D‐juveniles. Interestingly, these Vibrio sequences affiliated most closely with the coral pathogen, Vibrio coralliilyticus, which has been implicated in some coral disease outbreaks. In contrast, A. tenuis hosting ITS 1 type C1 Symbiodinium did not exhibit major bacterial shifts in the elevated temperature treatment, indicating a more stable bacterial community during thermal stress; concomitantly a decline (10%) in photochemical efficiency was minimal for this group. D juveniles that had been exposed to moderately elevated sea temperatures (30 °C) in the field before being placed in the control temperature treatment displayed a decrease in the number of Vibrio affiliated sequences and bacterial profiles shifted to become more similar to profiles of corals harbouring type C1 Symbiodinium. In combination, these results demonstrate that thermal stress can result in shifts in coral‐associated bacterial communities, which may lead to deteriorating coral health. The lower resilience of A. tenuis to thermal stress when harbouring Symbiodinium D highlights the importance of inter‐kingdom interactions among the coral host, dinoflagellate endosymbiont and bacterial associates for coral health and resilience.