Coral Reproduction in a Changing Climate

Coral Reproduction in a Changing Climate | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Coral Reproduction in a Changing Climate Jessica Bouwmeester, Jonathan Daly, Nikolas Zuchowicz, Claire Lager, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-1864235/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 05 Jan, 2023 Read the published version in Scientific Reports → Version 1 posted 8 You are reading this latest preprint version Abstract Coral reefs worldwide are at risk due to climate change. Coral bleaching is becoming increasingly common and corals that survive bleaching events can suffer from temporary reproductive failure for several years. While water temperature is a key driver in causing coral bleaching, other environmental factors are involved, such as solar radiation. We investigated the individual and combined effects of temperature, photosynthetically active radiation (PAR), and ultraviolet radiation (UVR) on the spawning patterns and reproductive physiology of the Hawaiʻian mushroom coral Lobactis scutaria , using long-term experiments in aquaria. We examined effects on spawning timing, fertilisation success, and gamete physiology. Both warmer temperatures and filtering UVR altered the timing of spawning. Warmer temperatures caused a drop in fertilisation success. Warmer temperatures and higher PAR both negatively affected sperm and egg physiology. Thermal stress from global climate change will need to be adequately addressed to ensure the survival of reef-building corals in their natural environment throughout the next century and beyond. Until then, reproduction is likely to be increasingly impaired. On a regional scale, some damage related to photo-oxidative stress may be partially mitigated through shading reefs or specific corals, to reduce bleaching, minimise the loss of coral fitness, and maintain coral reproduction. Broadcast Spawning Climate Change Computer Assisted Sperm Analysis Fungia scutaria Photosynthetically Active Radiation Seawater Temperature Spawning Synchrony Ultraviolet Radiation Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 Figure 8 Introduction Global climate change has pressed coral reefs around the world into an era of challenge and uncertainty. Coral reefs are among the oldest ecosystems on earth but are also some of the most vulnerable to climate change. They are habitats for a quarter of all marine life, they protect our coastlines and homes, and they feed over one seventh of the Earth’s human population 1 , 2 . However, they live at the upper limit of their thermal threshold, making them sensitive to even minimal increases in ocean temperatures 3 . Summer temperature anomalies in the last decades have regularly disrupted the fragile symbiosis between corals and their algal symbionts 4 , 5 , causing coral bleaching, with recurrent and stronger bleaching events expected in the coming decades. Climate change is altering coral reefs around the world, affecting the distribution, abundance and biodiversity of coral reef–associated organisms 6 . In order for corals to survive through the next decades, they must adapt their physiology and metabolism to new ocean circulation patterns, nutrient inputs, and oxygen contents, higher water temperatures, and lower pH 7 . Acclimation to environmental change can occur to some extent via phenotypic plasticity, but lasting, genetic adaptation can come about only by way of sexual reproduction and natural or selective breeding 8 – 10 . Today, all reefs have experienced some degree of bleaching due to climate change 11 , 12 and global restoration efforts strive to protect surviving reefs and restore damaged ones 13 – 16 . During bleaching, the coral hosts are deprived of their nutrient-providing algal symbionts (family Symbiodiniaceae) and slowly starve. If the surrounding environment returns to favourable conditions and the algal symbiont communities repopulate their hosts in time, the corals can recover. However, their overall fitness remains affected, with potentially detrimental long-term impacts. Typically, during coral bleaching, algal symbiont density and chlorophyll concentration are greatly decreased, leading to a drop in symbiont photosynthesis, decreased coral respiration and calcification, and a decline in coral lipids, carbohydrates, protein, and tissue biomass 17 – 21 . While metabolic processes such as algal symbiont photosynthesis and coral respiration can return to their pre-bleaching levels within 1–3 months once the source of bleaching is removed, in some species, energy reserves such as carbohydrates and proteins may require up to a year to recover 20 , 22 . Without the necessary energy reserves during the 6 to 11-month gametogenesis cycle observed by most scleractinian coral species 23 – 25 , coral reproduction can remain disturbed for a prolonged period. For example, gamete development can fail to complete 18,26−28 , fewer polyps may be fertile within a colony 29 , 30 , polyps may produce fewer gametes 18,28−31 , fertilisation success may decline 32 , 33 , or larval development may be abnormal 33 , 34 . In some cases, coral reproduction has required 4–5 years to recover and return to pre-bleaching levels 18 , 28 . Coral bleaching is without doubt a clear visual indicator of major environmental stress, but the absence of bleaching does not necessarily preclude stress. Indeed, lower levels of stress can negatively impact the health of corals without showing bleaching. Corals exposed to thermal stress below bleaching thresholds showed changes in the expression of possible stress indicator genes 35 , 36 , reduction in skeletal growth and impaired recovery from injuries 37 , damage to the morphology and physiology of the coral’s algal symbionts 38 , and a shift in the relation between the coral host and its symbionts, at the cost of the coral host’s health 39 . While thermal stress is viewed as the main cause of coral bleaching, other environmental factors can be involved as well; notably, solar radiation, both in the visible and the ultraviolet wavelengths, can significantly influence the severity of thermally-induced coral bleaching 40 , 41 . Solar radiation in the visible range (photosynthetically active radiation, PAR: 400–700 nm) is vital to photosynthetic organisms such as the algal symbionts that live within the tissue of reef-building corals; but at levels beyond the organism’s thresholds, the photosystem saturates, and harmful reactive oxygen species (ROS) are released, damaging the photosynthetic apparatus 42 – 44 . When both temperature and PAR light stress are present, two different pathways of cellular damage to the coral symbionts may interact, increasing the likelihood of a breakdown in the coral–symbiont symbiosis (i.e., coral bleaching) and the degree of that breakdown 45 – 47 . Solar radiation in the ultraviolet range (ultraviolet radiation, UVR: 280–400 nm) is overall understood to be detrimental to corals, with effects that include DNA damage, diminished metabolism, bleaching, mortality, and oxidative stress 48 . The cellular physiology and pathways involved during UVR-related stress alone are not fully understood but experiments that manipulated UVR alone revealed rapid lethal effects of full UVR exposure in the worst cases, and reduced growth and calcification in the best cases 49 , 50 . When both temperature and UVR stress are present, effects can be additive, causing a stronger response than would be expected by each stressor alone 51 , 52 . In the central Pacific archipelago of Hawaiʻi, two major bleaching events occurred in the summers of 2014 and 2015, resulting in widespread mortality across coral assemblages 53 , 54 . In Kāneʻohe Bay, on the island of Oʻahu, bleaching was extensive but the survival rates were high 55 . Nevertheless, reproductive physiology work conducted in Kāneʻohe Bay before, during and after the bleaching events, revealed that sperm motility in at least two coral species dropped nearly by half following the first bleaching event 33 and remained depressed for the following four years 33 , 56 . This suggests that the environmental stress that led to extensive coral bleaching in 2014 and 2015 may have caused long-term physiological damage, or perhaps some environmental stress remained, although at sub-bleaching levels. We here investigate the potential impact of climate change on the physiology of yearly coral reproductive events in an experimental system, examining both the individual and combined effects of temperature, ultraviolet radiation (UVR), and photosynthetically active radiation (PAR) in altering reproductive characteristics in coral. Environmental factors such as temperature and light are generally interconnected on the reef and it can be challenging to distinguish the different effects from each other. Therefore, we conducted these experiments in large flow-through aquaria and controlled the temperature, UVR, and PAR levels for 9 months prior to spawning, covering the entire gametogenesis cycle 57 and presumably altering the early reproductive characteristics of the coral. We report effects on the timing of spawning at the month, day, and time-of-day level. We report fertilisation success, sperm characteristics such as motility, duration of motility, and early apoptotic signals, and egg volume. Finally, we report changes in coral pigmentation that would indicate early stress levels on the coral holobiont, as well as changes in coral growth throughout the experiment. Methods Coral Collection and Husbandry All experiments were conducted on the scleractinian coral Lobactis scutaria , a sequential hermaphroditic, free-living solitary coral from the family Fungiidae, commonly found in Kāneʻohe Bay, Oahu, Hawaiʻi 58 , 59 . Spawning dates of L. scutaria in the region are highly reliable with spawning occurring monthly from June to September, 1–4 days after the full moon, in the evening between 17:00 and 19:00 33,58,60 . Two hundred L. scutaria individuals were collected on snorkel in Kāneʻohe Bay, Hawaiʻi, in 2015–2017, from a depth of 1–5 m, under permits to the Hawaiʻi Institute of Marine Biology # SAP 2015-17, SAP 2016-69, and SAP 2018-03, from the State of Hawaiʻi Department of Land & Natural Resources. The individuals were tagged and kept in captivity in shaded flow-through outdoor aquaria at the Hawaiʻi Institute of Marine Biology on Moku o Loʻe. All aquaria, before and during the experiment, contained yellow tangs ( Zebrasoma flavescens ) and threadfin butterflyfish ( Chaetodon auriga ) to control algae levels and to prevent pest outbreaks. Their diet was supplemented with nori seaweed and brine shrimp three times a week. Grazing fish were maintained under the supervision of the University of Hawaiʻi Office of Research Compliance with the Animal Care and Use Committee protocol # 14-1884-3. Experimental setup In late December 2017, prior to the onset of the 9-month-long gametogenesis cycle in L. scutaria 57 , all individuals were randomly assigned to one of eight treatment groups with 25 individual mushroom corals in each treatment (Fig. 1 ). The experimental factors were temperature (2 levels: historical (2008–2013) or current (2014–2019), with current temperature ~ 2°C higher than historical temperature on average in the summer months), ultraviolet radiation (UVR) (2 levels: ambient or 98% filtered), and photosynthetically active radiation (PAR) (2 levels: minimally (~ 5%) or partially (~ 35%) shaded). The eight treatments were spread into four large 850-litre outdoor tanks, with each tank containing two PAR levels. Within a tank, the two groups under different PAR treatments were separated by a 20-cm gap, to account for solar movement and ensure that all corals remained in their PAR treatment at any given time of day. All tanks were supplied by a continuous flow of warmed or chilled sand-filtered seawater, and were exposed to natural levels of sunshine and moonlight minus the UVR and PAR experimental filtering used in this experiment. Throughout the experiment, the temperature and the PAR levels were monitored on a bi-weekly basis to verify that the two levels of both factors were constant in each experimental treatment. Seawater temperatures in the Hawaiʻian Islands have gradually been increasing in the past decades 53,61−64 and in Kāneʻohe Bay, since the 2014 and 2015 bleaching events, they have remained higher than usual 65 . Therefore, we adjusted our two temperature treatments to follow pre-bleaching and post-bleaching temperature regimens, determined by 2008–2013 and 2014–2019 temperature data, respectively, from Kāneʻohe Bay (Fig. 2 a). These temperature regimens were retrieved from an automated weather station located on Moku o Lo‘e at the Hawai‘i Institute of Marine Biology (HIMB) ( http://www.pacioos.hawaii.edu/weather/obs-mokuoloe/ ), which collects hourly temperature data at 1 m depth. Treatment temperatures were controlled by a chilled water system and aquarium heaters when needed and were monitored throughout the experiments with temperature loggers collecting hourly data (Onset, HOBO). A daily average was extracted for all temperature data and the maxima and minima temperatures of each 5-year range of temperature data were used to visualise the temperature range during each period, in comparison with our treatment temperatures. UVR can cause substantial damage to corals 48 , 51 and therefore we wanted to test whether blocking UV radiation could prevent damage to the corals’ reproductive physiology. Half of the treatments were exposed to ambient UVR conditions and UVR was reduced by 98% in the other half, using ultraviolet-blocking acrylic sheets (MinPlastics, Honolulu, OP-3 acrylic sheet: blocks ~ 98% UVR at 200–400 nm with partial irradiance (~ 50%) blocked in the visible range at 400–430 nm). To visualise the UVR ranges for both treatments, UVR data were retrieved for the month of June 2018 from HIMB’s weather station ( http://www.pacioos.hawaii.edu/weather/obs-mokuoloe/ ), matching UVR conditions for the ambient UVR treatment, and for the UVR-shielded treatment UVR data were calculated as 2% of the ambient treatment (Fig. 2 b). PAR is a vital environmental input for corals that associate with photosynthetic organisms, as is true of most reef-building corals; but in excess it can cause damage to the algal symbionts’ photosystem apparatus and precipitate coral bleaching 66 – 68 . Similarly, in periods of high thermal stress, controlling PAR levels has been shown to help mitigate the effects of thermal stress by preventing additional release of damaging reactive oxygen species, thereby reducing damage to the coral symbionts’ photosynthesis apparatus and decreasing coral bleaching 69 – 71 . The two chosen PAR levels in the PAR treatments represented reductions from natural surface conditions (high PAR: ~5% PAR reduction, and low PAR: ~35% PAR reduction, determined with an underwater quantum flux reader, model MQ-210, Apogee), corresponding to conditions encountered on shallow reef flats/edges (~ 0.1–1 m) and shallow reef slopes (~ 2–3 m), respectively. PAR data were retrieved for the month of June 2018 from HIMB’s weather station ( http://www.pacioos.hawaii.edu/weather/obs-mokuoloe/ ) to visualise the PAR ranges for both PAR treatments. The treatment ranges were calculated as 95% and 65% of the ambient PAR values (Fig. 2 c). Spawning timing and gamete collection On the expected days of spawning (1–4 days after the full moons of June, July, and August), all 200 coral individuals were placed in individual 3-L containers at 15:45, shortly before the expected time of spawning, so that gametes could be collected for each individual. All coral individuals were closely monitored for spawning until 19:30, and those that spawned were recorded and their gametes were collected. Sperm was collected by transfer pipette immediately upon release from the mouths of the individual males. Eggs were left to settle in the bottom of the containers and were collected about one hour after release. Sperm physiology and fertilisation experiments were run during the month of August only and egg physiology was run in June, July, and August. Spawning synchrony Spawning synchrony was assessed for each treatment using the Marquis synchrony index adapted for coral reproduction 72 , 73 . The synchrony index, here calculated at the daily level, takes into account the proportion of corals spawning on each day that spawning was monitored. $${S}_{M}=\frac{{d}_{1}}{\sum _{t=1}^{t=n}{d}_{t}}\bullet {p}_{1}+\frac{{d}_{2}}{\sum _{t=1}^{t=n}{d}_{t}}\bullet {p}_{2}+\frac{{d}_{3}}{\sum _{t=1}^{t=n}{d}_{t}}\bullet {p}_{3}+\dots +\frac{{d}_{n}}{\sum _{t=1}^{t=n}{d}_{t}}\bullet {p}_{n}$$ where t is the day of spawning monitoring, n is the number of days monitored, d t is the number of corals spawning on day t , p t is the proportion of corals that spawned on day t , and \(\sum _{t=1}^{t=n}{d}_{t}\) is the total cumulative number of corals that spawned during the period studied. The Marquis index of synchrony ranges from 0 (spawning spread evenly across the spawning days) to 1 (all corals spawned synchronously on the same days). Fertilisation success Spawned eggs and sperm from each treatment were used in fertilisation experiments to assess the effects of temperature, UVR, and PAR on fertilisation success. In fertilisation experiments, eggs from 4–10 female fungiids per treatment were fertilised by a sperm pool of 1–6 male fungiids (number dependent on availability each night) from the same treatments following Hagedorn and co-authors 74 . Thirty to 150 eggs from each female were placed in individual scintillation vials containing 5 ml filtered seawater (FSW) and sperm from the sperm pool of their treatment was added (final sperm concentration: 1 × 10 6 cells/ml). After an hour incubation period to allow for fertilisation to occur, the number of eggs was counted under a dissecting microscope to determine the total number of eggs in each vial and the egg–sperm bath was diluted threefold. Fertilisation success was assessed ~ 12 hours later by counting the fertilised eggs under a dissecting microscope. Unfertilised eggs had dissociated by that time. Each fertilisation trial was paired with a control that was run similarly to the fertilisation trial but without sperm, to monitor for accidental fertilisation. Sperm physiology Sperm motility was assessed within five minutes after being collected, using computer-assisted sperm analysis (CASA; Hamilton Thorne, Ceros II System, Olympus BX41 with a 10× objective and green filter) system, following Zuchowicz and co-authors 75 . Motile sperm was differentiated from non-motile sperm using a movement threshold of 0.8, with sperm heads moving > 80% of their head diameter characterised as motile. For each sperm sample, a minimum of five video fields and 200 sperm cells were captured to determine total sperm motility. Sperm motility is often driven by sperm mitochondrial membrane potential 76 and therefore, to test whether this was the case here, a portion of the sperm was then tested for its mitochondrial function using a JC-1 stain assay (Accuri JC-1 Mitochondrial Potential Assay Kit KR310) and a flow cytometer (BD Accuri C6 Plus Flow Cytometer). Egg physiology The collected eggs were brought to the laboratory and imaged with a Science Supply camera mounted on an Olympus BX-41 microscope using a 20× objective and a 0.5× C mount. One to ten eggs were imaged from each individual. The images were analysed with ImageJ software (U.S. National Institutes of Health, version 1.52g) to obtain visible egg surface area, using the “Analyse particles” tool. The egg surface area was converted to egg volume, assuming sphericity. Egg volume followed a bimodal distribution due to the presence, in some female corals, of very small eggs that were prematurely released alongside mature eggs. A lower volume threshold was therefore set at 0.0007 mm 3 to remove the smaller egg population from the analysis. Statistical analyses were therefore run only on the larger egg population (0.0007–0.0030 mm 3 ). Coral Growth To examine differences in coral growth throughout the experiment, buoyant weight measurements 77 were taken at the beginning of the experiment (December 2017) and again at the end of the experiment (September 2018). Buoyant weights were converted to dry weights following Jokiel and co-authors 77 . The difference in dry weights was calculated for each coral and divided by the total number of days to find the average growth per day. Bleaching/paling response While our experimental design was not aimed at causing a full bleaching response in our corals, we expected the high temperature, high UVR and high PAR treatments to cause sufficient stress to induce some loss in symbionts, resulting in some visible paling of the coral hosts. Photographic images of each coral were taken at the beginning (Dec 2017) and at the end (Sep 2018) of the experiment, using an Olympus TG-6 compact camera, with fixed lighting, fixed object distance, and manual camera settings to ensure uniform capture conditions. The images were converted to greyscale for analysis in ImageJ, which calculated the average brightness for each coral (black = 0, white = 255). Brightness values were compared between the beginning and the end of the experiment, yielding a percent increase in colour brightness as indicator of coral bleaching. Statistical analyses To fulfil normality assumptions, square-root and lognormal transformations were used to normalise percentage data and measurement data, respectively. Mixed-model Analyses of Variance (ANOVA) with temperature, UVR, and PAR as fixed factors were used to test their individual and interactive effects on the timing of spawning and the physiology of the gametes. Normality of the residuals was verified by plotting a histogram of the residuals against a normal distribution curve and homoscedasticity was verified by plotting the model residuals against the fitted model. A mixed-model ANOVA with four fixed factors was conducted on egg sizes, with the month of spawning included as the fourth factor. Sperm physiology data was considered from the month of August only due to different sampling designs in other months. Where relevant, post hoc tests were conducted with least square means pairwise comparisons with Tukey adjustment for multiple comparisons. Two-way ordinal regressions with cumulative link models were used to test for a shift in spawning months among the treatments. The relation between sperm motility and percent high mitochondrial membrane potential was assessed with Pearson’s correlation test. All statistical analyses were conducted using R 78 and the R packages car 79 , ggplot2 80 , lsmeans 81 , multcomp 82 , multcompView 83 , ordinal 84 , rcompanion 85 , Rmisc 86 , and RVAideMemoire 87 . Results Spawning timing and synchrony Spawning occurred in June, July, and August, in the week following the full moon. The number of spawning days per individual ranged from 0 to 7, with an average of 3.19 ± 0.11 days (mean ± standard error) (Supplementary Table S1). However, the number of days during which each coral spawned was affected by both temperature and UVR (mixed-model ANOVA, F (1,188) = 13.9, p-value = 3×10 − 4 and F (1,188) = 22.4, p-value = 4×10 − 6 , respectively, Fig. 3 a, Supplementary Table S2). Current temperature regimens caused a drop in the number of spawning days compared to historical temperatures, and blocking 95% UVR caused a similar drop in the number of spawning days (Fig. 3 a). Additionally, temperature and UVR had a significant interaction effect (mixed-model ANOVA, F (1,188) = 6.6, p-value = 0.01, Fig. 3 a, Supplementary Table S2), with historical temperatures and ambient UVR causing a significantly higher number of spawning days than any other combination (post hoc test: least square means with Tukey correction). Within each treatment, spawning synchrony determined by the Marquis index 72 , 73 , ranged from 0.50 to 0.72 (scale: 0 to 1). The lowest synchrony occurred at current (warmer) temperature regimens with UVR filtered out and 5% shaded PAR, and the highest synchrony was found at historical (lower) temperatures, ambient UVR and 35% shaded PAR (Fig. 3 b). Overall, synchrony appeared to be the most affected when temperature and PAR were on the higher end, and when UVR was filtered out. Overall, 62% of fungiid corals first spawned in the month of June in 2018 (Supplementary Table S1). However, the onset of spawning at the month level was affected by both temperature (two-way ordinal regression, χ 2 = 38.2, p = 2×10 − 9 ) and UVR (two-way ordinal regression, χ 2 = 6.8, p = 0.028), with current (warmer) temperatures and ambient UVR increasing the proportion of corals that first spawned in the month of June, and historical (lower) temperatures and blocked UVR increasing the number of corals that shifted the onset of spawning to the month of July (Fig. 3 c; Supplementary Table S3). Throughout the 2018 summer months, spawning was observed between 16:00 and 18:30 (Supplementary Table S1). The time of day that spawning started was affected both by the month (mixed-model ANOVA, F (1,385) = 30.9, p = 5×10 − 8 ) and by temperature (mixed-model ANOVA, F (1,385) = 602.5, p < 2×10 − 16 ) (Supplementary Table S4). Spawning in July was delayed by 40 min on average relative to June, and the temperature caused on average an 80-min delay in spawning with corals at current (higher) temperatures spawning earlier than the corals at historical (lower) temperatures (Fig. 3 d). Interactive effects were also noted between temperature and month (mixed-model ANOVA, F (1,385) = 7.7, p = 0.006), with temperature having a stronger effect in July than in June, and between UVR and month (mixed-model ANOVA, F (1,385) = 8.1, p = 0.005), with ambient UVR causing a delay in spawning time in June but not in July (Fig. 3 d; Supplementary Table S4). Data from the month of August were not included in the statistical analysis. In August, exceptional conditions (i.e. Hurricane Lane 88 ), forced us to evacuate all corals out of their treatments and into a single solid emergency aquarium that was less likely to be destroyed in case of a direct hit by the hurricane, for a period of three days. After three days, the corals were returned to their treatments and monitored that same day for spawning. No significant month effect was observed between July and August (corals spawned on average only 4 min later). However, the delay between temperature treatments had disappeared (under high temperatures, spawning started only 4 min earlier than under lower temperatures). Fertilisation success Fertilisation success within treatments was overall 85 ± 3% (mean ± standard error) (Supplementary Table S5). Current (warmer) temperatures decreased fertilisation success (three-way ANOVA, F (1,52) = 4.8, p = 0.033) to 80% on average in the warmer treatments. Fertilisation success was also impacted by combined effects of temperature and PAR (mixed-model ANOVA, F (1,52) = 5.0, p = 0.029), and by the combined effects of temperature, PAR and UVR (mixed-model ANOVA, F (1,52) = 6.9, p = 0.011, Fig. 4 ; Supplementary Table S6). Sperm physiology Sperm motility, assessed by CASA, ranged from 26–95% (Supplementary Table S7) and was significantly affected by PAR, with the 35% shaded PAR treatment increasing sperm motility from 61% (average motility in the 5% shaded PAR treatment) to 73% (Fig. 5 a; Supplementary Table S8). Differences in sperm motility can often be explained by changes in sperm mitochondrial membrane potential (MMP). High MMP is generally expected but low MMP would reveal some damage to the sperm. The percentage of corals with high sperm MMP was highly variable, ranging from 25–92% (Supplementary Table S7). Unlike sperm motility, MMP was affected by temperature (mixed-model ANOVA, F (1,37) = 7.2, p = 0.011) with a higher proportion of corals with high MMP at current (warmer) temperatures in comparison to historical temperatures, respectively 66% and 51% on average (Fig. 5 b; Supplementary Table S9). Sperm motility and high mitochondrial membrane potential were not significantly correlated (Fig. 5 c, Pearson’s correlation, r = 0.19, t (43) = 1.3, p = 0.198). Egg physiology The size of the eggs released by L. scutaria was significantly affected by temperature, PAR, and the month of spawning (mixed-model ANOVA, F (1,175) = 68.9, p = 3×10 − 14 , four-way ANOVA, F (1,175) = 6.4, p = 0.012, mixed-model ANOVA, F (2,175) = 5.2, p = 0.006, respectively; Supplementary Table S11). Current (warmer) temperature reduced egg size by 14%, ambient PAR reduced egg size by 3%, and in June, eggs were 10% smaller than in July and August (Fig. 6 ; Supplementary Table S10). Coral Growth A 21% reduction in growth was observed at higher temperature (mixed-model ANOVA, F (1,186) = 11.2, p = 0.001; Fig. 7 ; Tables S12–13). Temperature and UVR had a significant interactive effect on growth with the highest growth at low temperature and ambient UVR (mixed-model ANOVA, F (1,186) = 8.6, p = 0.004; Fig. 7 ; Supplementary Table S13). Bleaching/paling response Considering all treatments together, corals paled by 12 ± 1% (mean ± standard error) between December 2017 and September 2018 (Supplementary Table S12). Nevertheless, the change in coral pigmentation was affected by temperature, UVR, and PAR (mixed-model ANOVA, F (1,191) = 93.9, p < 2×10 − 16 ; mixed-model ANOVA, F (1,191) = 18.4, p = 3×10 − 5 ; mixed-model ANOVA, F (1,191) = 23.5, p = 3×10 − 6 , respectively; Supplementary Table S14). Current (higher) temperature caused 18% paling, ambient PAR caused 15% paling, and blocked UVR caused 14% paling (Fig. 8 ). Discussion Temperature, ultraviolet radiation (UVR) and photosynthetically active radiation (PAR), all played significant but different roles in affecting the reproductive biology of the coral L. scutaria . The present study showed that timing of spawning was affected by higher temperature and blocked UVR but not by PAR. Reproductive success was affected by higher temperature, and sperm and egg physiology were affected both by temperature and PAR. Growth was affected by temperature, and corals paled more at the higher levels of temperature and PAR and when UVR was filtered out. The interactions of thermal stress with light stress both at the PAR level and UVR level are clearly complex, but understanding the individual role of each factor, and understanding how they interact, provides vital information to understand how to manage these stressors in the changing environment that we are expecting in the coming decades. Sessile animals such as corals rely on the synchronous release of gametes from different genotypes to cross-fertilise and produce viable offspring 89 , 90 . We found that the number of opportunities for cross-fertilisation (i.e. total number of spawning days) dropped with warmer temperatures and when UVR was blocked. Similarly, we found that spawning synchrony, determined with the Marquis synchrony index, also dropped in a warmer temperature regimen and when UVR was blocked. Higher synchrony occurred in conditions that yielded a higher number of spawning days, and synchrony dropped when conditions yielded a drop in number of spawning days. This relationship can happen when the number and proportion of corals involved in spawning is high on each day 73 . Indeed, the higher the synchrony and the more opportunities for a high proportion of the coral population to spawn on the same day, the higher the chances of reproductive success on the reef 91 . The opposite trend (i.e. high number of spawning days related to low synchrony) was recently suggested to occur in coral communities in Eilat, northern Red Sea 92 , but the authors did not quantify synchrony directly and instead, qualitatively inferred synchrony from other reproductive metrics, without taking into account the proportion of corals that spawned in the population, without which synchrony cannot be determined 93 . In our case, in Hawai‘i, we found that an increase in temperature yielded fewer spawning days and a drop in spawning synchrony. Oceans around the globe have been warming steadily since the 1970s 94 , 95 and are likely to continue warming in the next decades 96 , potentially affecting spawning synchrony throughout coral populations globally in the coming years. We found that spawning synchrony was also lower when UVR was blocked. Corals are believed to follow lunar cues to determine the days of spawning, which involves detecting low levels of blue light, which is adjacent to the ultraviolet spectrum 97 – 99 . Blocking UVR in half of our treatments may have affected those corals’ ability to detect the lunar cues in the blue range, which corals use to time their days of spawning. It is also possible that the lunar cues needed for spawning synchrony may overlap with the longer wavelengths of the ultraviolet range. Both warmer temperature regimens and ambient UVR caused a proportion of corals to start spawning a month earlier. By shifting the onset of spawning to an earlier month, these corals can spawn in better thermal conditions, showing potential for a favourable adaptation to warming conditions. A similar shift in the month of spawning has been reported in Acropora japonica (but not in A. hyacinthus ), in Favites pentagona , and in Platygyra contorta in Japan, where spawning occurred a month earlier when seawater temperatures were higher than average during the last three months of gametogenesis 100 . In addition to a month shift in the onset of spawning, we found that warmer temperatures caused a shift in the time of day that spawning begins, with corals exposed to higher temperatures spawning 80 min earlier on average. Most scleractinian corals spawn at night, in the hours following sunset, but L. scutaria spawns in the late afternoon, presumably not using the sunset as a proximate cue for the time of spawning as night-spawning corals do 101 – 103 . While adapting to warming temperature by advancing the onset of spawning to an earlier month is advantageous in avoiding hotter water temperatures, spawning earlier in the afternoon will cause gametes to be released at a time of the day when the water is warmer and insolation is stronger. Hotter- than-normal temperatures at the time of gamete release can reduce fertilisation success, cause abnormalities in developing larvae, and reduce larval survival 104 , 105 . In addition, stronger insolation can lead to DNA damage to the gametes and developing larvae due to stronger ultraviolet radiation 48 , 106 , 107 . While this effect is alarming, we found that the shift in spawning to earlier in the afternoon caused by higher water temperature can be reset in just three days, as we accidentally found out when we had to evacuate all corals to a safer tank due to Hurricane Lane in August 2018. While the exact mechanisms by which the fungiid corals synchronise their spawning to the same time of day remain unknown, we found that water temperature played a significant role, either as a direct cue, or through disrupting the mechanisms responsible for determining the timing. Fertilisation success is highly dependent on a sufficiently high concentration of motile sperm 32 , 75 . Once above a minimum ratio threshold of 5×10 3 sperm per egg for the coral L. scutaria 75 , fertilisation is generally high, which is likely why we obtained high fertilisation success in all treatments. Higher temperature caused a drop in fertilisation success with the lowest fertilisation rates observed at warmer temperature, low PAR and ambient UVR. A few studies have investigated the effect of short-term increased temperature during the stages of fertilisation success and larval development in corals and have found that an increase in temperature during these stages tended to accelerate the duration of larval development 104 but did not necessarily cause a drop in fertilisation success, except in Acropora millepora 104 . In the coral A. tenuis , the sperm concentration threshold necessary for successful fertilisation was found to be possibly higher at increased temperatures, requiring approximately a 6- to 8-fold higher sperm concentration at 3°C above ambient temperatures in the coral A. tenuis 108 . However, the authors did not evaluate sperm motility, so the need for increased sperm concentration could simply have been to compensate for lower sperm motility at higher temperature to obtain similar fertilisation success rates. Following bleaching events, drops in fertilisation have been apparent in several coral species 32 , 33 , but many confounding effects other than temperature could have been involved. The present study is the first that tests the independent effect of temperature over a period of several months, here encompassing the full gametogenesis cycle, on reproductive success. Our results confirm that the effects of temperature and other coral bleaching-related environmental stressors such as solar radiation on fertilisation success can remain minimal as long as sperm concentration is high. Some temperature effect was noted, but we would suggest further studies using lower concentrations of motile sperm to identify the limits of fertilisation success under different levels of environmental stress. Unlike fertilisation success, sperm motility dropped at high PAR and was not affected by temperature. The lack of correlation with temperature suggests that although some sperm motility is important for fertilisation success, here other factors may be involved. For example, we found the strongest effect on egg volume to be temperature, with a drop in egg size at warmer temperatures. The smaller eggs might have been the cause of the reduced fertilisation success in the higher temperature treatments. Sperm motility has been overall low since two consecutive bleaching events in Hawaiʻi in 2014 and 2015 33 . Loss of sperm motility is paired with a loss in sperm mitochondrial membrane potential (MMP) in humans 109 , 110 and bovines 111 , but also in marine invertebrates such as sea urchins 76 , 112 and in some coral species 56 . Indeed, a high proportion of high MMP reflects the process of electron transport and oxidative phosphorylation, the driving force behind ATP production and therefore sperm motility. However, this relationship was not found in sperm from marine ascidians or mussels; loss of sperm motility was instead correlated to reactive oxygen species levels and plasma membrane lipid peroxidation 111 . Similarly, in sperm from the coral L. scutaria , we found no relation between MMP and sperm motility. Here, the cause of the loss of sperm motility is therefore elsewhere. That sperm motility was diminished at high PAR suggests that the stress that primarily drove sperm motility here likely occurred at the level of the symbiont, the photosynthetic partner in the symbiosis, during spermatogenesis. Several studies report negative effects from UVR or combined UVR and PAR on the sperm motility of corals 113 and other marine invertebrates 114 , 115 , but few from PAR alone. In a study comparing DNA damage, a sign of advanced cell apoptosis, in coral larvae with and without symbionts when exposed to direct insolation (high PAR and high UVR were coupled), DNA damage was higher in larvae with symbionts than in larvae without symbionts, indicating that the symbionts were the source of oxidative stress 116 . To understand how oxidative stress in the symbionts led to a decrease in sperm motility, further work testing gene expression regulatory mechanisms is needed, possibly with high resolution imaging to identify any morphological anomalies. Testing the direct effects of reactive oxygen species, the toxic compound released during photo-oxidative stress, on sperm cells, during their development or after their release, might also provide valuable answers. The volume of the eggs released by female L. scutaria individuals was reduced at warmer temperatures, but it also dropped at higher PAR and was lower in the first month of spawning (i.e. June). A similar temperature effect was found in the coral Acropora digitifera in Okinawa when exposed to temperature regimens 2°C above ambient temperatures over several weeks prior to spawning 117 . Eggs are mostly composed of lipids, which will act as energy reserves for the developing larva. To build up enough lipids to produce larger eggs, sufficient resources need to be available. These are provided by the photosynthetic symbionts as part of their symbiotic relationship with their coral host, which relies on the symbionts being healthy and abundant. In this study we found that both temperature and PAR caused corals to pale, which indicates that the symbionts were at the very least less abundant and likely not able to provide as many nutrients to their coral host as their counterparts in the lower temperature and PAR treatments. Although warmer temperatures, PAR, and UVR all caused paling of corals, coral growth was affected only by the warmer temperature treatments that represent recent temperature observations on reefs in Kāneʻohe Bay (based on data 2014–2019). Previous work in Kāneʻohe Bay has shown that the optimal temperature for coral calcification, including for L. scutaria , is 25.9°C and that coral growth drops when above that threshold 118 . Our results confirm these earlier results but alarmingly suggest that coral growth might be already dropping throughout Kāneʻohe Bay due to ocean warming. Elsewhere, reductions in coral growth linked with warming ocean temperatures have already been detected in the Red Sea 119 , on the Great Barrier Reef 120 , in the Andaman Sea 121 , 122 , and in the South China Sea 122 . The physiological effects of global climate change on coral reproduction are numerous and complex. However, the bottom line is that without robust reproduction, corals may not be able to adapt to changing ocean conditions. We show that warming ocean temperatures and high solar radiation both negatively affect the reproductive physiology of the mushroom coral L. scutaria , but they may do so through different cellular pathways. Oceans are predicted to continue warming in the decades to come, which will likely cause a further reduction in coral spawning synchrony, disrupt the timing of spawning, cause a further drop in fertilisation success and in egg volume, and slow coral growth. To manage warming ocean temperatures will take a global effort and strong political will and action, but that effort is necessary to prevent the loss of coral reefs and the vital ecosystems services that they provide 123 . While high levels of PAR are likely to continue to affect the reproductive physiology of corals in the coming decades, artificially controlling PAR levels may be an effective option to reduce damage to sperm and eggs, and to mitigate bleaching effects under thermal stress. Shading corals has been tested for a variety of coral species, showing promising results in reducing coral bleaching and decreasing effects on overall fitness 71 . Our results suggest that it could also prevent damage to coral gametes, thus reducing the risk of reproductive failure. Shading can be managed at a local level, targeting coral reefs of special interest, as sole intervention or in conjunction with other interventions such as enhancing coral recruitment or implementing assisted gene flow 10 , 124 , 125 . Finally, high levels of ultraviolet radiation are known to cause cellular damage in many organisms but lower levels of UVR may play an important functional role. Here, we show that completely blocking UVR can impair lunar cycle–related cues, on which the corals rely for determining the timing of spawning and maintaining spawning synchrony. The coming decades will be challenging for coral reefs around the world, but one of the key steps to conserving reef-building corals, will be to ensure that reproduction is maintained. This will require global, annual monitoring of coral reproduction. If reproductive issues are anticipated, measures can be put in place to aid reproductive events on a regional scale through mitigating environmental stress, e.g., by shading reefs or specific corals. On a longer time-scale, global pressures from climate change will need to be addressed for oceans to return to thermal conditions more suitable for the world’s coral reefs to thrive again. Declarations Data Availability Statement The data supporting the findings of this paper are available in the article and Supplementary Information. Acknowledgements This research was supported by funds from the Smithsonian Institution, the Smithsonian Conservation Biology Institute, the Hawaiʻi Institute of Marine Biology, the Paul M. Angell Family Foundation, the Roddenberry Foundation, the Seaver Institute, the William H. Donner Foundation, the Barrett Family Foundation, the Skippy Frank Foundation, the Compton Foundation, the Cedar Hill Foundation, the Anela Kolohe Foundation, and the Smithsonian Women’s Committee. The authors would like to thank Katherine Hardy, Brock Wetzlich, and Ned Busch, for assisting with spawning observations and gamete collection. This manuscript was given an HIMB contribution # XXX. Author Contributions JB, JD, NH, CL, EMH, and MH conceived the ideas and designed the methodology. JB, JD, NH, CL, EMH, MQ, and MH collected the data. JB and MH analysed the data and wrote a first draft of the manuscript. All authors provided critical feedback to the manuscript and approved the submitted version. 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Toxicol. 97 , 3–14 (2010). Nesa, B., Baird, A. H., Harii, S., Yakovleva, I. & Hidaka, M. Algal symbionts increase DNA damage in coral planulae exposed to sunlight. Zool. Stud. 51 , 12–17 (2012). Paxton, C. W., Baria, M. V. B., Weis, V. M. & Harii, S. Effect of elevated temperature on fecundity and reproductive timing in the coral Acropora digitifera . Zygote 24 , 511 (2015). Jokiel, P. & Coles, S. Effects of temperature on the mortality and growth of Hawaiian reef corals. Mar. Biol. 43 , 201–208 (1977). Cantin, N. E., Cohen, A. L., Karnauskas, K. B., Tarrant, A. M. & McCorkle, D. C. Ocean warming slows coral growth in the Central Red Sea. Science 329 , 322–325, doi: 10.1126/science.1190182 (2010). Cooper, T. F., De'Ath, G., Fabricius, K. E. & Lough, J. M. Declining coral calcification in massive Porites in two nearshore regions of the northern Great Barrier Reef. Glob. Chang. Biol. 14 , 529–538 (2008). Tanzil, J., Brown, B., Tudhope, A. & Dunne, R. Decline in skeletal growth of the coral Porites lutea from the Andaman Sea, South Thailand between 1984 and 2005. Coral Reefs 28 , 519–528 (2009). Tanzil, J. T. I. et al. Regional decline in growth rates of massive Porites corals in Southeast Asia. Glob. Chang. Biol. 19 , 3011–3023 (2013). Chen, P.-Y., Chen, C.-C., Chu, L. & McCarl, B. Evaluating the economic damage of climate change on global coral reefs. Glob. Environ. Change 30 , 12–20 (2015). Anthony, K. R. et al. Interventions to help coral reefs under global change—A complex decision challenge. PloS One 15 , e0236399 (2020). Daly, J. et al. Cryopreservation can assist gene flow on the Great Barrier Reef. Coral Reefs 41 , 455–462 (2022). Additional Declarations No competing interests reported. Supplementary Files SupplementaryInformation20220629.pdf Cite Share Download PDF Status: Published Journal Publication published 05 Jan, 2023 Read the published version in Scientific Reports → Version 1 posted Editorial decision: Major revision 29 Aug, 2022 Reviews received at journal 15 Aug, 2022 Reviewers agreed at journal 26 Jul, 2022 Reviewers invited by journal 22 Jul, 2022 Editor assigned by journal 21 Jul, 2022 Editor invited by journal 21 Jul, 2022 Submission checks completed at journal 21 Jul, 2022 First submitted to journal 16 Jul, 2022 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-1864235","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":122811900,"identity":"d9a34e93-632f-46d3-8d8b-30e2ad403106","order_by":0,"name":"Jessica Bouwmeester","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA1ElEQVRIiWNgGAWjYBACAxTOBwYJIJVApBYeIDacQbIWZh4wk4AWc/YeM6kbFTb29uy9D4pt/lgw8LPnGODVYtlzxkw650xaYg/PcQPj3DYJBsmeN/i1GNzIMbud23Y4gUcijcE4t0ECJEKMln//7XnknzEYW/yRYLAnTkvDAcYeCTYGYwY2oC0SBP1yrPx3zrHkxJ4zaQyGvW0SPBJnnhXg1WLO3rzZOKfGzp69/RibwY8/dXL87ckb8GpBBmwgB/EQrRwEmB+QpHwUjIJRMApGDAAACD4/WHllM1sAAAAASUVORK5CYII=","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Jessica","middleName":"","lastName":"Bouwmeester","suffix":""},{"id":122811903,"identity":"96d6782a-949c-4ff4-9a4d-cf0c7a77da8d","order_by":1,"name":"Jonathan Daly","email":"","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Jonathan","middleName":"","lastName":"Daly","suffix":""},{"id":122811904,"identity":"a5b3d010-7ec5-437c-bc89-bed2b1c1255c","order_by":2,"name":"Nikolas Zuchowicz","email":"","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Nikolas","middleName":"","lastName":"Zuchowicz","suffix":""},{"id":122811905,"identity":"488053fa-b9b5-44b0-8514-e2739cc882ea","order_by":3,"name":"Claire Lager","email":"","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Claire","middleName":"","lastName":"Lager","suffix":""},{"id":122811906,"identity":"17285a3c-94eb-4d6e-a98f-16b6fd9831f1","order_by":4,"name":"E. Michael Henley","email":"","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"E.","middleName":"Michael","lastName":"Henley","suffix":""},{"id":122811907,"identity":"ef0894d6-9cf6-4778-be08-bef9a72a6374","order_by":5,"name":"Mariko Quinn","email":"","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Mariko","middleName":"","lastName":"Quinn","suffix":""},{"id":122811908,"identity":"9fbb2bae-159e-41a8-88b6-dd3c0b421b64","order_by":6,"name":"Mary Hagedorn","email":"","orcid":"","institution":"Smithsonian Conservation Biology Institute, Front Royal","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Mary","middleName":"","lastName":"Hagedorn","suffix":""}],"badges":[],"createdAt":"2022-07-16 10:14:14","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-1864235/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-1864235/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1038/s41598-022-27207-6","type":"published","date":"2023-01-05T18:13:58+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":24422782,"identity":"b20326f0-9e56-4310-814a-b7818ec1a8fe","added_by":"auto","created_at":"2022-07-27 19:57:27","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":1177177,"visible":true,"origin":"","legend":"\u003cp\u003eSummary of experimental conditions and number of \u003cem\u003eL. scutaria\u003c/em\u003e individuals per treatment. A total of 200 individuals was divided into eight treatments, each exposed to one of two levels of temperature, ultraviolet radiation (UVR), and photosynthetically active radiation (PAR). Current temperature regimens are based on empirical data from 2014–2019 and historical temperatures are based on data from 2008–2013. Filtered UVR is 98% filtered. High PAR is 5% shaded and low PAR is 35% shaded.\u0026nbsp;\u003c/p\u003e","description":"","filename":"1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/1bc26c5b730ba5d10273aca5.jpg"},{"id":24422736,"identity":"2bf73dd9-18dd-49b9-83dc-4007b6b5c4ea","added_by":"auto","created_at":"2022-07-27 19:52:27","extension":"jpg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":1616216,"visible":true,"origin":"","legend":"\u003cp\u003e(a) Seawater temperatures in the higher and lower temperature treatments (solid lines) following historical temperature ranges from the Moku o Loʻe weather station from pre-bleaching years (2008–2013) and post-bleaching years (2014–2019, includes bleaching years) (lighter coloured ranges). (b) Ultraviolet ranges in the ambient UVR and 98% blocked UVR treatments visualised here for the month of June 2018, based on records from the Moku o Loʻe weather station. (c) Photosynthetically active radiation ranges in the 5% and 35% shaded treatments, in comparison to ambient PAR levels recorded at the Moku o Loʻe weather station in June 2018.\u0026nbsp;\u003c/p\u003e","description":"","filename":"2.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/740f98c820e246acc724fa82.jpg"},{"id":24422738,"identity":"e8557fff-4fad-43d9-b3a0-da3d7854c475","added_by":"auto","created_at":"2022-07-27 19:52:27","extension":"jpg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":1886022,"visible":true,"origin":"","legend":"\u003cp\u003eEffects of seawater temperature, PAR, and UV radiation on the timing of coral spawning. \u003cstrong\u003e(a)\u003c/strong\u003e Both temperature and UVR affected the total number of spawning days (mean ± SE) that \u003cem\u003eL. scutaria\u003c/em\u003e spawned in summer 2018. Low (historical) temperature and ambient UVR yielded the highest number of spawning days. \u003cstrong\u003e(b)\u003c/strong\u003e Spawning synchrony was determined with the Marquis Index for each of the eight treatments, and is ranked from low to high synchrony. The lowest synchrony was found at high (current) temperature, low UVR and ambient PAR, and the highest synchrony was found at low (historical) temperature, ambient UVR, and low PAR. \u003cstrong\u003e(c)\u003c/strong\u003e Both temperature and UVR affected the first month of spawning of \u003cem\u003eL. scutaria\u003c/em\u003e. High temperature and ambient UVR both independently yielded a shift in the initial month of spawning, increasing the percentage of corals sparting their spawning period in June rather than July. \u003cstrong\u003e(d)\u003c/strong\u003e Both temperature and the spawning month had direct effects on the time of day that \u003cem\u003eLobactis scutaria\u003c/em\u003e spawned. Present-day temperatures caused corals to spawn earlier than those at historical temperatures and spawning occurred later in July in comparison to June. UVR significantly interacted with the month of spawning but did not have a direct effect on the time of spawning. Treatments that share the same letter are not significantly different from each other.\u003c/p\u003e","description":"","filename":"3.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/d551ed63c92560fb918db83c.jpg"},{"id":24422739,"identity":"fbd0868f-6627-43f0-a417-a7c603036cca","added_by":"auto","created_at":"2022-07-27 19:52:27","extension":"jpg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":916843,"visible":true,"origin":"","legend":"\u003cp\u003eFertilisation success was directly impacted only by temperature, with a reduction in percent fertilisation at current-day temperatures. UVR and PAR had significant interactive effects with temperature but did not show any direct effect on fertilisation. Treatments that share the same letter are not significantly different from each other.\u003c/p\u003e","description":"","filename":"4.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/c40dfbeec407b9005a20efbc.jpg"},{"id":24422735,"identity":"e32f77d6-dd5b-443c-8c57-95f4e7cf765b","added_by":"auto","created_at":"2022-07-27 19:52:27","extension":"jpg","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":1066985,"visible":true,"origin":"","legend":"\u003cp\u003eSperm physiology was affected by PAR and temperature. Sperm motility \u003cstrong\u003e(a)\u003c/strong\u003e was sensitive to PAR and was lower at ambient PAR levels. Mitochondrial membrane potential \u003cstrong\u003e(b)\u003c/strong\u003e was sensitive to temperature and was lower at historical (low) temperature levels. A star \u003cstrong\u003e*\u003c/strong\u003e means that the treatments were significantly different from each other. \u003cstrong\u003e(c)\u003c/strong\u003e There was no significant correlation between percent sperm with high mitochondrial membrane potential and percent sperm motility (p = 0.198)\u003c/p\u003e","description":"","filename":"5.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/4c0da5485b584270f6730c9f.jpg"},{"id":24422741,"identity":"25f2850f-c6c5-4a21-8d30-c940abafc87d","added_by":"auto","created_at":"2022-07-27 19:52:28","extension":"jpg","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":885460,"visible":true,"origin":"","legend":"\u003cp\u003eThe size of the eggs that were released each month was affected by temperature \u003cstrong\u003e(a)\u003c/strong\u003e, PAR \u003cstrong\u003e(b)\u003c/strong\u003e, and the month that the eggs were released \u003cstrong\u003e(c)\u003c/strong\u003e. Present-day temperatures yielded a smaller egg size, as did ambient PAR levels. In June, the eggs were smaller than in July and August. A star \u003cstrong\u003e*\u003c/strong\u003e means that the treatments were significantly different from each other. Treatments that share the same letter are not significantly different from each other.\u003c/p\u003e","description":"","filename":"6.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/ea48215f749fd97d1a48a409.jpg"},{"id":24422742,"identity":"6805ccdb-64b7-4bd0-92a5-8a261e6a4eb8","added_by":"auto","created_at":"2022-07-27 19:52:28","extension":"jpg","order_by":7,"title":"Figure 7","display":"","copyAsset":false,"role":"figure","size":791141,"visible":true,"origin":"","legend":"\u003cp\u003eCoral growth was affected by temperature, with reduced growth at present-day temperature regimens. UVR interacted with temperature but did not have a direct effect on growth. Treatments that share the same letter are not significantly different from each other.\u003c/p\u003e","description":"","filename":"7.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/9771996ec2ff2d17377f0f81.jpg"},{"id":24422783,"identity":"601ee9ee-9b6d-459e-8f35-f41c29808adf","added_by":"auto","created_at":"2022-07-27 19:57:28","extension":"jpg","order_by":8,"title":"Figure 8","display":"","copyAsset":false,"role":"figure","size":990350,"visible":true,"origin":"","legend":"\u003cp\u003eSome degree of coral paling occurred in all treatments between December 2017 and September 2018. However, corals paled significantly more at high temperature \u003cstrong\u003e(a)\u003c/strong\u003e, when UVR was filtered out \u003cstrong\u003e(b)\u003c/strong\u003e, and at ambient PAR levels \u003cstrong\u003e(c)\u003c/strong\u003e. A star \u003cstrong\u003e*\u003c/strong\u003e means that the treatments were significantly different from each other.\u003c/p\u003e","description":"","filename":"8.jpg","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/01a37c4473419aad79cdba15.jpg"},{"id":44715835,"identity":"c46b4ee4-e02d-48e5-b87d-7000f32cd0b1","added_by":"auto","created_at":"2023-10-16 18:18:49","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1115614,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/e79d1d39-1bbd-4459-9665-00b221cc10f2.pdf"},{"id":24422734,"identity":"c6899c7c-382f-440d-9676-cdfd9a4104fb","added_by":"auto","created_at":"2022-07-27 19:52:27","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":238761,"visible":true,"origin":"","legend":"","description":"","filename":"SupplementaryInformation20220629.pdf","url":"https://assets-eu.researchsquare.com/files/rs-1864235/v1/b16f270311733dc1e1a62747.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Coral Reproduction in a Changing Climate","fulltext":[{"header":"Introduction","content":"\u003cp\u003eGlobal climate change has pressed coral reefs around the world into an era of challenge and uncertainty. Coral reefs are among the oldest ecosystems on earth but are also some of the most vulnerable to climate change. They are habitats for a quarter of all marine life, they protect our coastlines and homes, and they feed over one seventh of the Earth\u0026rsquo;s human population \u003csup\u003e\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e,\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e\u003c/sup\u003e. However, they live at the upper limit of their thermal threshold, making them sensitive to even minimal increases in ocean temperatures \u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e. Summer temperature anomalies in the last decades have regularly disrupted the fragile symbiosis between corals and their algal symbionts \u003csup\u003e\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e,\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e\u003c/sup\u003e, causing coral bleaching, with recurrent and stronger bleaching events expected in the coming decades. Climate change is altering coral reefs around the world, affecting the distribution, abundance and biodiversity of coral reef\u0026ndash;associated organisms \u003csup\u003e\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u003c/sup\u003e. In order for corals to survive through the next decades, they must adapt their physiology and metabolism to new ocean circulation patterns, nutrient inputs, and oxygen contents, higher water temperatures, and lower pH \u003csup\u003e\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e\u003c/sup\u003e. Acclimation to environmental change can occur to some extent via phenotypic plasticity, but lasting, genetic adaptation can come about only by way of sexual reproduction and natural or selective breeding \u003csup\u003e\u003cspan additionalcitationids=\"CR9\" citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eToday, all reefs have experienced some degree of bleaching due to climate change \u003csup\u003e\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e,\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u003c/sup\u003e and global restoration efforts strive to protect surviving reefs and restore damaged ones \u003csup\u003e\u003cspan additionalcitationids=\"CR14 CR15\" citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e\u003c/sup\u003e. During bleaching, the coral hosts are deprived of their nutrient-providing algal symbionts (family Symbiodiniaceae) and slowly starve. If the surrounding environment returns to favourable conditions and the algal symbiont communities repopulate their hosts in time, the corals can recover. However, their overall fitness remains affected, with potentially detrimental long-term impacts. Typically, during coral bleaching, algal symbiont density and chlorophyll concentration are greatly decreased, leading to a drop in symbiont photosynthesis, decreased coral respiration and calcification, and a decline in coral lipids, carbohydrates, protein, and tissue biomass \u003csup\u003e\u003cspan additionalcitationids=\"CR18 CR19 CR20\" citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e\u003c/sup\u003e. While metabolic processes such as algal symbiont photosynthesis and coral respiration can return to their pre-bleaching levels within 1\u0026ndash;3 months once the source of bleaching is removed, in some species, energy reserves such as carbohydrates and proteins may require up to a year to recover \u003csup\u003e\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e,\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e\u003c/sup\u003e. Without the necessary energy reserves during the 6 to 11-month gametogenesis cycle observed by most scleractinian coral species \u003csup\u003e\u003cspan additionalcitationids=\"CR24\" citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e\u003c/sup\u003e, coral reproduction can remain disturbed for a prolonged period. For example, gamete development can fail to complete \u003csup\u003e18,26\u0026minus;28\u003c/sup\u003e, fewer polyps may be fertile within a colony \u003csup\u003e\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e,\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e\u003c/sup\u003e, polyps may produce fewer gametes \u003csup\u003e18,28\u0026minus;31\u003c/sup\u003e, fertilisation success may decline \u003csup\u003e\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e,\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e\u003c/sup\u003e, or larval development may be abnormal \u003csup\u003e\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e,\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e\u003c/sup\u003e. In some cases, coral reproduction has required 4\u0026ndash;5 years to recover and return to pre-bleaching levels \u003csup\u003e\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e,\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eCoral bleaching is without doubt a clear visual indicator of major environmental stress, but the absence of bleaching does not necessarily preclude stress. Indeed, lower levels of stress can negatively impact the health of corals without showing bleaching. Corals exposed to thermal stress below bleaching thresholds showed changes in the expression of possible stress indicator genes \u003csup\u003e\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e,\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e\u003c/sup\u003e, reduction in skeletal growth and impaired recovery from injuries \u003csup\u003e\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e\u003c/sup\u003e, damage to the morphology and physiology of the coral\u0026rsquo;s algal symbionts \u003csup\u003e\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e\u003c/sup\u003e, and a shift in the relation between the coral host and its symbionts, at the cost of the coral host\u0026rsquo;s health \u003csup\u003e\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eWhile thermal stress is viewed as the main cause of coral bleaching, other environmental factors can be involved as well; notably, solar radiation, both in the visible and the ultraviolet wavelengths, can significantly influence the severity of thermally-induced coral bleaching \u003csup\u003e\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e,\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e\u003c/sup\u003e. Solar radiation in the visible range (photosynthetically active radiation, PAR: 400\u0026ndash;700 nm) is vital to photosynthetic organisms such as the algal symbionts that live within the tissue of reef-building corals; but at levels beyond the organism\u0026rsquo;s thresholds, the photosystem saturates, and harmful reactive oxygen species (ROS) are released, damaging the photosynthetic apparatus \u003csup\u003e\u003cspan additionalcitationids=\"CR43\" citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e44\u003c/span\u003e\u003c/sup\u003e. When both temperature and PAR light stress are present, two different pathways of cellular damage to the coral symbionts may interact, increasing the likelihood of a breakdown in the coral\u0026ndash;symbiont symbiosis (i.e., coral bleaching) and the degree of that breakdown \u003csup\u003e\u003cspan additionalcitationids=\"CR46\" citationid=\"CR45\" class=\"CitationRef\"\u003e45\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e47\u003c/span\u003e\u003c/sup\u003e. Solar radiation in the ultraviolet range (ultraviolet radiation, UVR: 280\u0026ndash;400 nm) is overall understood to be detrimental to corals, with effects that include DNA damage, diminished metabolism, bleaching, mortality, and oxidative stress \u003csup\u003e\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e\u003c/sup\u003e. The cellular physiology and pathways involved during UVR-related stress alone are not fully understood but experiments that manipulated UVR alone revealed rapid lethal effects of full UVR exposure in the worst cases, and reduced growth and calcification in the best cases \u003csup\u003e\u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e49\u003c/span\u003e,\u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e50\u003c/span\u003e\u003c/sup\u003e. When both temperature and UVR stress are present, effects can be additive, causing a stronger response than would be expected by each stressor alone \u003csup\u003e\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e,\u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e52\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eIn the central Pacific archipelago of Hawaiʻi, two major bleaching events occurred in the summers of 2014 and 2015, resulting in widespread mortality across coral assemblages \u003csup\u003e\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e53\u003c/span\u003e,\u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e54\u003c/span\u003e\u003c/sup\u003e. In Kāneʻohe Bay, on the island of Oʻahu, bleaching was extensive but the survival rates were high \u003csup\u003e\u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e55\u003c/span\u003e\u003c/sup\u003e. Nevertheless, reproductive physiology work conducted in Kāneʻohe Bay before, during and after the bleaching events, revealed that sperm motility in at least two coral species dropped nearly by half following the first bleaching event \u003csup\u003e\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e\u003c/sup\u003e and remained depressed for the following four years \u003csup\u003e\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e,\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e. This suggests that the environmental stress that led to extensive coral bleaching in 2014 and 2015 may have caused long-term physiological damage, or perhaps some environmental stress remained, although at sub-bleaching levels.\u003c/p\u003e \u003cp\u003eWe here investigate the potential impact of climate change on the physiology of yearly coral reproductive events in an experimental system, examining both the individual and combined effects of temperature, ultraviolet radiation (UVR), and photosynthetically active radiation (PAR) in altering reproductive characteristics in coral. Environmental factors such as temperature and light are generally interconnected on the reef and it can be challenging to distinguish the different effects from each other. Therefore, we conducted these experiments in large flow-through aquaria and controlled the temperature, UVR, and PAR levels for 9 months prior to spawning, covering the entire gametogenesis cycle \u003csup\u003e\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u003c/sup\u003e and presumably altering the early reproductive characteristics of the coral. We report effects on the timing of spawning at the month, day, and time-of-day level. We report fertilisation success, sperm characteristics such as motility, duration of motility, and early apoptotic signals, and egg volume. Finally, we report changes in coral pigmentation that would indicate early stress levels on the coral holobiont, as well as changes in coral growth throughout the experiment.\u003c/p\u003e"},{"header":"Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eCoral Collection and Husbandry\u003c/h2\u003e \u003cp\u003eAll experiments were conducted on the scleractinian coral \u003cem\u003eLobactis scutaria\u003c/em\u003e, a sequential hermaphroditic, free-living solitary coral from the family Fungiidae, commonly found in Kāneʻohe Bay, Oahu, Hawaiʻi \u003csup\u003e\u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e58\u003c/span\u003e,\u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e59\u003c/span\u003e\u003c/sup\u003e. Spawning dates of \u003cem\u003eL. scutaria\u003c/em\u003e in the region are highly reliable with spawning occurring monthly from June to September, 1\u0026ndash;4 days after the full moon, in the evening between 17:00 and 19:00 \u003csup\u003e33,58,60\u003c/sup\u003e. Two hundred \u003cem\u003eL. scutaria\u003c/em\u003e individuals were collected on snorkel in Kāneʻohe Bay, Hawaiʻi, in 2015\u0026ndash;2017, from a depth of 1\u0026ndash;5 m, under permits to the Hawaiʻi Institute of Marine Biology # SAP 2015-17, SAP 2016-69, and SAP 2018-03, from the State of Hawaiʻi Department of Land \u0026amp; Natural Resources. The individuals were tagged and kept in captivity in shaded flow-through outdoor aquaria at the Hawaiʻi Institute of Marine Biology on Moku o Loʻe. All aquaria, before and during the experiment, contained yellow tangs (\u003cem\u003eZebrasoma flavescens\u003c/em\u003e) and threadfin butterflyfish (\u003cem\u003eChaetodon auriga\u003c/em\u003e) to control algae levels and to prevent pest outbreaks. Their diet was supplemented with nori seaweed and brine shrimp three times a week. Grazing fish were maintained under the supervision of the University of Hawaiʻi Office of Research Compliance with the Animal Care and Use Committee protocol # 14-1884-3.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eExperimental setup\u003c/h2\u003e \u003cp\u003eIn late December 2017, prior to the onset of the 9-month-long gametogenesis cycle in \u003cem\u003eL. scutaria\u003c/em\u003e \u003csup\u003e\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e57\u003c/span\u003e\u003c/sup\u003e, all individuals were randomly assigned to one of eight treatment groups with 25 individual mushroom corals in each treatment (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The experimental factors were temperature (2 levels: historical (2008\u0026ndash;2013) or current (2014\u0026ndash;2019), with current temperature\u0026thinsp;~\u0026thinsp;2\u0026deg;C higher than historical temperature on average in the summer months), ultraviolet radiation (UVR) (2 levels: ambient or 98% filtered), and photosynthetically active radiation (PAR) (2 levels: minimally (~\u0026thinsp;5%) or partially (~\u0026thinsp;35%) shaded). The eight treatments were spread into four large 850-litre outdoor tanks, with each tank containing two PAR levels. Within a tank, the two groups under different PAR treatments were separated by a 20-cm gap, to account for solar movement and ensure that all corals remained in their PAR treatment at any given time of day. All tanks were supplied by a continuous flow of warmed or chilled sand-filtered seawater, and were exposed to natural levels of sunshine and moonlight minus the UVR and PAR experimental filtering used in this experiment. Throughout the experiment, the temperature and the PAR levels were monitored on a bi-weekly basis to verify that the two levels of both factors were constant in each experimental treatment.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eSeawater temperatures in the Hawaiʻian Islands have gradually been increasing in the past decades \u003csup\u003e53,61\u0026minus;64\u003c/sup\u003e and in Kāneʻohe Bay, since the 2014 and 2015 bleaching events, they have remained higher than usual \u003csup\u003e\u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e65\u003c/span\u003e\u003c/sup\u003e. Therefore, we adjusted our two temperature treatments to follow pre-bleaching and post-bleaching temperature regimens, determined by 2008\u0026ndash;2013 and 2014\u0026ndash;2019 temperature data, respectively, from Kāneʻohe Bay (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ea). These temperature regimens were retrieved from an automated weather station located on Moku o Lo\u0026lsquo;e at the Hawai\u0026lsquo;i Institute of Marine Biology (HIMB) (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://www.pacioos.hawaii.edu/weather/obs-mokuoloe/\u003c/span\u003e\u003cspan address=\"http://www.pacioos.hawaii.edu/weather/obs-mokuoloe/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e), which collects hourly temperature data at 1 m depth. Treatment temperatures were controlled by a chilled water system and aquarium heaters when needed and were monitored throughout the experiments with temperature loggers collecting hourly data (Onset, HOBO). A daily average was extracted for all temperature data and the maxima and minima temperatures of each 5-year range of temperature data were used to visualise the temperature range during each period, in comparison with our treatment temperatures.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eUVR can cause substantial damage to corals \u003csup\u003e\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e,\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e51\u003c/span\u003e\u003c/sup\u003e and therefore we wanted to test whether blocking UV radiation could prevent damage to the corals\u0026rsquo; reproductive physiology. Half of the treatments were exposed to ambient UVR conditions and UVR was reduced by 98% in the other half, using ultraviolet-blocking acrylic sheets (MinPlastics, Honolulu, OP-3 acrylic sheet: blocks\u0026thinsp;~\u0026thinsp;98% UVR at 200\u0026ndash;400 nm with partial irradiance (~\u0026thinsp;50%) blocked in the visible range at 400\u0026ndash;430 nm). To visualise the UVR ranges for both treatments, UVR data were retrieved for the month of June 2018 from HIMB\u0026rsquo;s weather station (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://www.pacioos.hawaii.edu/weather/obs-mokuoloe/\u003c/span\u003e\u003cspan address=\"http://www.pacioos.hawaii.edu/weather/obs-mokuoloe/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e), matching UVR conditions for the ambient UVR treatment, and for the UVR-shielded treatment UVR data were calculated as 2% of the ambient treatment (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eb).\u003c/p\u003e \u003cp\u003ePAR is a vital environmental input for corals that associate with photosynthetic organisms, as is true of most reef-building corals; but in excess it can cause damage to the algal symbionts\u0026rsquo; photosystem apparatus and precipitate coral bleaching \u003csup\u003e\u003cspan additionalcitationids=\"CR67\" citationid=\"CR66\" class=\"CitationRef\"\u003e66\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e68\u003c/span\u003e\u003c/sup\u003e. Similarly, in periods of high thermal stress, controlling PAR levels has been shown to help mitigate the effects of thermal stress by preventing additional release of damaging reactive oxygen species, thereby reducing damage to the coral symbionts\u0026rsquo; photosynthesis apparatus and decreasing coral bleaching \u003csup\u003e\u003cspan additionalcitationids=\"CR70\" citationid=\"CR69\" class=\"CitationRef\"\u003e69\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e71\u003c/span\u003e\u003c/sup\u003e. The two chosen PAR levels in the PAR treatments represented reductions from natural surface conditions (high PAR: ~5% PAR reduction, and low PAR: ~35% PAR reduction, determined with an underwater quantum flux reader, model MQ-210, Apogee), corresponding to conditions encountered on shallow reef flats/edges (~\u0026thinsp;0.1\u0026ndash;1 m) and shallow reef slopes (~\u0026thinsp;2\u0026ndash;3 m), respectively. PAR data were retrieved for the month of June 2018 from HIMB\u0026rsquo;s weather station (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://www.pacioos.hawaii.edu/weather/obs-mokuoloe/\u003c/span\u003e\u003cspan address=\"http://www.pacioos.hawaii.edu/weather/obs-mokuoloe/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e) to visualise the PAR ranges for both PAR treatments. The treatment ranges were calculated as 95% and 65% of the ambient PAR values (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003ec).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eSpawning timing and gamete collection\u003c/h2\u003e \u003cp\u003eOn the expected days of spawning (1\u0026ndash;4 days after the full moons of June, July, and August), all 200 coral individuals were placed in individual 3-L containers at 15:45, shortly before the expected time of spawning, so that gametes could be collected for each individual. All coral individuals were closely monitored for spawning until 19:30, and those that spawned were recorded and their gametes were collected. Sperm was collected by transfer pipette immediately upon release from the mouths of the individual males. Eggs were left to settle in the bottom of the containers and were collected about one hour after release. Sperm physiology and fertilisation experiments were run during the month of August only and egg physiology was run in June, July, and August.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eSpawning synchrony\u003c/h2\u003e \u003cp\u003eSpawning synchrony was assessed for each treatment using the Marquis synchrony index adapted for coral reproduction \u003csup\u003e\u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e72\u003c/span\u003e,\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e\u003c/sup\u003e. The synchrony index, here calculated at the daily level, takes into account the proportion of corals spawning on each day that spawning was monitored.\u003cdiv id=\"Equa\" class=\"Equation\"\u003e\u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equa\" name=\"EquationSource\"\u003e\n$${S}_{M}=\\frac{{d}_{1}}{\\sum _{t=1}^{t=n}{d}_{t}}\\bullet {p}_{1}+\\frac{{d}_{2}}{\\sum _{t=1}^{t=n}{d}_{t}}\\bullet {p}_{2}+\\frac{{d}_{3}}{\\sum _{t=1}^{t=n}{d}_{t}}\\bullet {p}_{3}+\\dots +\\frac{{d}_{n}}{\\sum _{t=1}^{t=n}{d}_{t}}\\bullet {p}_{n}$$\u003c/div\u003e\u003c/div\u003e\u003c/p\u003e \u003cp\u003ewhere \u003cem\u003et\u003c/em\u003e is the day of spawning monitoring, \u003cem\u003en\u003c/em\u003e is the number of days monitored, \u003cem\u003ed\u003c/em\u003e\u003csub\u003e\u003cem\u003et\u003c/em\u003e\u003c/sub\u003e is the number of corals spawning on day \u003cem\u003et\u003c/em\u003e, \u003cem\u003ep\u003c/em\u003e\u003csub\u003e\u003cem\u003et\u003c/em\u003e\u003c/sub\u003e is the proportion of corals that spawned on day \u003cem\u003et\u003c/em\u003e, and \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\sum _{t=1}^{t=n}{d}_{t}\\)\u003c/span\u003e\u003c/span\u003e is the total cumulative number of corals that spawned during the period studied. The Marquis index of synchrony ranges from 0 (spawning spread evenly across the spawning days) to 1 (all corals spawned synchronously on the same days).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eFertilisation success\u003c/h2\u003e \u003cp\u003eSpawned eggs and sperm from each treatment were used in fertilisation experiments to assess the effects of temperature, UVR, and PAR on fertilisation success. In fertilisation experiments, eggs from 4\u0026ndash;10 female fungiids per treatment were fertilised by a sperm pool of 1\u0026ndash;6 male fungiids (number dependent on availability each night) from the same treatments following Hagedorn and co-authors \u003csup\u003e\u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e74\u003c/span\u003e\u003c/sup\u003e. Thirty to 150 eggs from each female were placed in individual scintillation vials containing 5 ml filtered seawater (FSW) and sperm from the sperm pool of their treatment was added (final sperm concentration: 1 \u0026times; 10\u003csup\u003e6\u003c/sup\u003e cells/ml). After an hour incubation period to allow for fertilisation to occur, the number of eggs was counted under a dissecting microscope to determine the total number of eggs in each vial and the egg\u0026ndash;sperm bath was diluted threefold. Fertilisation success was assessed\u0026thinsp;~\u0026thinsp;12 hours later by counting the fertilised eggs under a dissecting microscope. Unfertilised eggs had dissociated by that time. Each fertilisation trial was paired with a control that was run similarly to the fertilisation trial but without sperm, to monitor for accidental fertilisation.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eSperm physiology\u003c/h2\u003e \u003cp\u003eSperm motility was assessed within five minutes after being collected, using computer-assisted sperm analysis (CASA; Hamilton Thorne, Ceros II System, Olympus BX41 with a 10\u0026times; objective and green filter) system, following Zuchowicz and co-authors \u003csup\u003e\u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e75\u003c/span\u003e\u003c/sup\u003e. Motile sperm was differentiated from non-motile sperm using a movement threshold of 0.8, with sperm heads moving\u0026thinsp;\u0026gt;\u0026thinsp;80% of their head diameter characterised as motile. For each sperm sample, a minimum of five video fields and 200 sperm cells were captured to determine total sperm motility. Sperm motility is often driven by sperm mitochondrial membrane potential \u003csup\u003e\u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e76\u003c/span\u003e\u003c/sup\u003e and therefore, to test whether this was the case here, a portion of the sperm was then tested for its mitochondrial function using a JC-1 stain assay (Accuri JC-1 Mitochondrial Potential Assay Kit KR310) and a flow cytometer (BD Accuri C6 Plus Flow Cytometer).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eEgg physiology\u003c/h2\u003e \u003cp\u003eThe collected eggs were brought to the laboratory and imaged with a Science Supply camera mounted on an Olympus BX-41 microscope using a 20\u0026times; objective and a 0.5\u0026times; C mount. One to ten eggs were imaged from each individual. The images were analysed with ImageJ software (U.S. National Institutes of Health, version 1.52g) to obtain visible egg surface area, using the \u0026ldquo;Analyse particles\u0026rdquo; tool. The egg surface area was converted to egg volume, assuming sphericity. Egg volume followed a bimodal distribution due to the presence, in some female corals, of very small eggs that were prematurely released alongside mature eggs. A lower volume threshold was therefore set at 0.0007 mm\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e to remove the smaller egg population from the analysis. Statistical analyses were therefore run only on the larger egg population (0.0007\u0026ndash;0.0030 mm\u003csup\u003e\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u003c/sup\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eCoral Growth\u003c/h2\u003e \u003cp\u003eTo examine differences in coral growth throughout the experiment, buoyant weight measurements \u003csup\u003e\u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e77\u003c/span\u003e\u003c/sup\u003e were taken at the beginning of the experiment (December 2017) and again at the end of the experiment (September 2018). Buoyant weights were converted to dry weights following Jokiel and co-authors \u003csup\u003e\u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e77\u003c/span\u003e\u003c/sup\u003e. The difference in dry weights was calculated for each coral and divided by the total number of days to find the average growth per day.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eBleaching/paling response\u003c/h2\u003e \u003cp\u003eWhile our experimental design was not aimed at causing a full bleaching response in our corals, we expected the high temperature, high UVR and high PAR treatments to cause sufficient stress to induce some loss in symbionts, resulting in some visible paling of the coral hosts. Photographic images of each coral were taken at the beginning (Dec 2017) and at the end (Sep 2018) of the experiment, using an Olympus TG-6 compact camera, with fixed lighting, fixed object distance, and manual camera settings to ensure uniform capture conditions. The images were converted to greyscale for analysis in ImageJ, which calculated the average brightness for each coral (black\u0026thinsp;=\u0026thinsp;0, white\u0026thinsp;=\u0026thinsp;255). Brightness values were compared between the beginning and the end of the experiment, yielding a percent increase in colour brightness as indicator of coral bleaching.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analyses\u003c/h2\u003e \u003cp\u003eTo fulfil normality assumptions, square-root and lognormal transformations were used to normalise percentage data and measurement data, respectively. Mixed-model Analyses of Variance (ANOVA) with temperature, UVR, and PAR as fixed factors were used to test their individual and interactive effects on the timing of spawning and the physiology of the gametes. Normality of the residuals was verified by plotting a histogram of the residuals against a normal distribution curve and homoscedasticity was verified by plotting the model residuals against the fitted model. A mixed-model ANOVA with four fixed factors was conducted on egg sizes, with the month of spawning included as the fourth factor. Sperm physiology data was considered from the month of August only due to different sampling designs in other months. Where relevant, post hoc tests were conducted with least square means pairwise comparisons with Tukey adjustment for multiple comparisons. Two-way ordinal regressions with cumulative link models were used to test for a shift in spawning months among the treatments. The relation between sperm motility and percent high mitochondrial membrane potential was assessed with Pearson\u0026rsquo;s correlation test. All statistical analyses were conducted using R \u003csup\u003e\u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e78\u003c/span\u003e\u003c/sup\u003e and the R packages car \u003csup\u003e\u003cspan citationid=\"CR79\" class=\"CitationRef\"\u003e79\u003c/span\u003e\u003c/sup\u003e, ggplot2 \u003csup\u003e80\u003c/sup\u003e, lsmeans \u003csup\u003e\u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e81\u003c/span\u003e\u003c/sup\u003e, multcomp \u003csup\u003e\u003cspan citationid=\"CR82\" class=\"CitationRef\"\u003e82\u003c/span\u003e\u003c/sup\u003e, multcompView \u003csup\u003e\u003cspan citationid=\"CR83\" class=\"CitationRef\"\u003e83\u003c/span\u003e\u003c/sup\u003e, ordinal \u003csup\u003e\u003cspan citationid=\"CR84\" class=\"CitationRef\"\u003e84\u003c/span\u003e\u003c/sup\u003e, rcompanion \u003csup\u003e\u003cspan citationid=\"CR85\" class=\"CitationRef\"\u003e85\u003c/span\u003e\u003c/sup\u003e, Rmisc \u003csup\u003e\u003cspan citationid=\"CR86\" class=\"CitationRef\"\u003e86\u003c/span\u003e\u003c/sup\u003e, and RVAideMemoire \u003csup\u003e\u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e87\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec14\" class=\"Section2\"\u003e \u003ch2\u003eSpawning timing and synchrony\u003c/h2\u003e \u003cp\u003eSpawning occurred in June, July, and August, in the week following the full moon. The number of spawning days per individual ranged from 0 to 7, with an average of 3.19\u0026thinsp;\u0026plusmn;\u0026thinsp;0.11 days (mean\u0026thinsp;\u0026plusmn;\u0026thinsp;standard error) (Supplementary Table S1). However, the number of days during which each coral spawned was affected by both temperature and UVR (mixed-model ANOVA, F\u003csub\u003e(1,188)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;13.9, p-value\u0026thinsp;=\u0026thinsp;3\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;4\u003c/sup\u003e and F\u003csub\u003e(1,188)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;22.4, p-value\u0026thinsp;=\u0026thinsp;4\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;6\u003c/sup\u003e, respectively, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea, Supplementary Table S2). Current temperature regimens caused a drop in the number of spawning days compared to historical temperatures, and blocking 95% UVR caused a similar drop in the number of spawning days (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea). Additionally, temperature and UVR had a significant interaction effect (mixed-model ANOVA, F\u003csub\u003e(1,188)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;6.6, p-value\u0026thinsp;=\u0026thinsp;0.01, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea, Supplementary Table S2), with historical temperatures and ambient UVR causing a significantly higher number of spawning days than any other combination (post hoc test: least square means with Tukey correction).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eWithin each treatment, spawning synchrony determined by the Marquis index \u003csup\u003e\u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e72\u003c/span\u003e,\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e\u003c/sup\u003e, ranged from 0.50 to 0.72 (scale: 0 to 1). The lowest synchrony occurred at current (warmer) temperature regimens with UVR filtered out and 5% shaded PAR, and the highest synchrony was found at historical (lower) temperatures, ambient UVR and 35% shaded PAR (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eb). Overall, synchrony appeared to be the most affected when temperature and PAR were on the higher end, and when UVR was filtered out.\u003c/p\u003e \u003cp\u003eOverall, 62% of fungiid corals first spawned in the month of June in 2018 (Supplementary Table S1). However, the onset of spawning at the month level was affected by both temperature (two-way ordinal regression, χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;38.2, p\u0026thinsp;=\u0026thinsp;2\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;9\u003c/sup\u003e) and UVR (two-way ordinal regression, χ\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;6.8, p\u0026thinsp;=\u0026thinsp;0.028), with current (warmer) temperatures and ambient UVR increasing the proportion of corals that first spawned in the month of June, and historical (lower) temperatures and blocked UVR increasing the number of corals that shifted the onset of spawning to the month of July (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ec; Supplementary Table S3).\u003c/p\u003e \u003cp\u003eThroughout the 2018 summer months, spawning was observed between 16:00 and 18:30 (Supplementary Table S1). The time of day that spawning started was affected both by the month (mixed-model ANOVA, F\u003csub\u003e(1,385)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;30.9, p\u0026thinsp;=\u0026thinsp;5\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;8\u003c/sup\u003e) and by temperature (mixed-model ANOVA, F\u003csub\u003e(1,385)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;602.5, p\u0026thinsp;\u0026lt;\u0026thinsp;2\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;16\u003c/sup\u003e) (Supplementary Table S4). Spawning in July was delayed by 40 min on average relative to June, and the temperature caused on average an 80-min delay in spawning with corals at current (higher) temperatures spawning earlier than the corals at historical (lower) temperatures (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ed). Interactive effects were also noted between temperature and month (mixed-model ANOVA, F\u003csub\u003e(1,385)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;7.7, p\u0026thinsp;=\u0026thinsp;0.006), with temperature having a stronger effect in July than in June, and between UVR and month (mixed-model ANOVA, F\u003csub\u003e(1,385)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;8.1, p\u0026thinsp;=\u0026thinsp;0.005), with ambient UVR causing a delay in spawning time in June but not in July (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ed; Supplementary Table S4). Data from the month of August were not included in the statistical analysis. In August, exceptional conditions (i.e. Hurricane Lane \u003csup\u003e\u003cspan citationid=\"CR88\" class=\"CitationRef\"\u003e88\u003c/span\u003e\u003c/sup\u003e), forced us to evacuate all corals out of their treatments and into a single solid emergency aquarium that was less likely to be destroyed in case of a direct hit by the hurricane, for a period of three days. After three days, the corals were returned to their treatments and monitored that same day for spawning. No significant month effect was observed between July and August (corals spawned on average only 4 min later). However, the delay between temperature treatments had disappeared (under high temperatures, spawning started only 4 min earlier than under lower temperatures).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eFertilisation success\u003c/h2\u003e \u003cp\u003eFertilisation success within treatments was overall 85\u0026thinsp;\u0026plusmn;\u0026thinsp;3% (mean\u0026thinsp;\u0026plusmn;\u0026thinsp;standard error) (Supplementary Table S5). Current (warmer) temperatures decreased fertilisation success (three-way ANOVA, F\u003csub\u003e(1,52)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;4.8, p\u0026thinsp;=\u0026thinsp;0.033) to 80% on average in the warmer treatments. Fertilisation success was also impacted by combined effects of temperature and PAR (mixed-model ANOVA, F\u003csub\u003e(1,52)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;5.0, p\u0026thinsp;=\u0026thinsp;0.029), and by the combined effects of temperature, PAR and UVR (mixed-model ANOVA, F\u003csub\u003e(1,52)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;6.9, p\u0026thinsp;=\u0026thinsp;0.011, Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e; Supplementary Table S6).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003eSperm physiology\u003c/h2\u003e \u003cp\u003eSperm motility, assessed by CASA, ranged from 26\u0026ndash;95% (Supplementary Table S7) and was significantly affected by PAR, with the 35% shaded PAR treatment increasing sperm motility from 61% (average motility in the 5% shaded PAR treatment) to 73% (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ea; Supplementary Table S8). Differences in sperm motility can often be explained by changes in sperm mitochondrial membrane potential (MMP). High MMP is generally expected but low MMP would reveal some damage to the sperm. The percentage of corals with high sperm MMP was highly variable, ranging from 25\u0026ndash;92% (Supplementary Table S7). Unlike sperm motility, MMP was affected by temperature (mixed-model ANOVA, F\u003csub\u003e(1,37)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;7.2, p\u0026thinsp;=\u0026thinsp;0.011) with a higher proportion of corals with high MMP at current (warmer) temperatures in comparison to historical temperatures, respectively 66% and 51% on average (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003eb; Supplementary Table S9). Sperm motility and high mitochondrial membrane potential were not significantly correlated (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ec, Pearson\u0026rsquo;s correlation, r\u0026thinsp;=\u0026thinsp;0.19, t\u003csub\u003e(43)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;1.3, p\u0026thinsp;=\u0026thinsp;0.198).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec17\" class=\"Section2\"\u003e \u003ch2\u003eEgg physiology\u003c/h2\u003e \u003cp\u003eThe size of the eggs released by \u003cem\u003eL. scutaria\u003c/em\u003e was significantly affected by temperature, PAR, and the month of spawning (mixed-model ANOVA, F\u003csub\u003e(1,175)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;68.9, p\u0026thinsp;=\u0026thinsp;3\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;14\u003c/sup\u003e, four-way ANOVA, F\u003csub\u003e(1,175)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;6.4, p\u0026thinsp;=\u0026thinsp;0.012, mixed-model ANOVA, F\u003csub\u003e(2,175)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;5.2, p\u0026thinsp;=\u0026thinsp;0.006, respectively; Supplementary Table S11). Current (warmer) temperature reduced egg size by 14%, ambient PAR reduced egg size by 3%, and in June, eggs were 10% smaller than in July and August (Fig.\u0026nbsp;\u003cspan refid=\"Fig6\" class=\"InternalRef\"\u003e6\u003c/span\u003e; Supplementary Table S10).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec18\" class=\"Section2\"\u003e \u003ch2\u003eCoral Growth\u003c/h2\u003e \u003cp\u003eA 21% reduction in growth was observed at higher temperature (mixed-model ANOVA, F\u003csub\u003e(1,186)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;11.2, p\u0026thinsp;=\u0026thinsp;0.001; Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003e; Tables S12\u0026ndash;13). Temperature and UVR had a significant interactive effect on growth with the highest growth at low temperature and ambient UVR (mixed-model ANOVA, F\u003csub\u003e(1,186)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;8.6, p\u0026thinsp;=\u0026thinsp;0.004; Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003e; Supplementary Table S13).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec19\" class=\"Section2\"\u003e \u003ch2\u003eBleaching/paling response\u003c/h2\u003e \u003cp\u003eConsidering all treatments together, corals paled by 12\u0026thinsp;\u0026plusmn;\u0026thinsp;1% (mean\u0026thinsp;\u0026plusmn;\u0026thinsp;standard error) between December 2017 and September 2018 (Supplementary Table S12). Nevertheless, the change in coral pigmentation was affected by temperature, UVR, and PAR (mixed-model ANOVA, F\u003csub\u003e(1,191)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;93.9, p\u0026thinsp;\u0026lt;\u0026thinsp;2\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;16\u003c/sup\u003e; mixed-model ANOVA, F\u003csub\u003e(1,191)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;18.4, p\u0026thinsp;=\u0026thinsp;3\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;5\u003c/sup\u003e; mixed-model ANOVA, F\u003csub\u003e(1,191)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;23.5, p\u0026thinsp;=\u0026thinsp;3\u0026times;10\u003csup\u003e\u0026minus;\u0026thinsp;6\u003c/sup\u003e, respectively; Supplementary Table S14). Current (higher) temperature caused 18% paling, ambient PAR caused 15% paling, and blocked UVR caused 14% paling (Fig.\u0026nbsp;\u003cspan refid=\"Fig8\" class=\"InternalRef\"\u003e8\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eTemperature, ultraviolet radiation (UVR) and photosynthetically active radiation (PAR), all played significant but different roles in affecting the reproductive biology of the coral \u003cem\u003eL. scutaria\u003c/em\u003e. The present study showed that timing of spawning was affected by higher temperature and blocked UVR but not by PAR. Reproductive success was affected by higher temperature, and sperm and egg physiology were affected both by temperature and PAR. Growth was affected by temperature, and corals paled more at the higher levels of temperature and PAR and when UVR was filtered out. The interactions of thermal stress with light stress both at the PAR level and UVR level are clearly complex, but understanding the individual role of each factor, and understanding how they interact, provides vital information to understand how to manage these stressors in the changing environment that we are expecting in the coming decades.\u003c/p\u003e \u003cp\u003eSessile animals such as corals rely on the synchronous release of gametes from different genotypes to cross-fertilise and produce viable offspring \u003csup\u003e\u003cspan citationid=\"CR89\" class=\"CitationRef\"\u003e89\u003c/span\u003e,\u003cspan citationid=\"CR90\" class=\"CitationRef\"\u003e90\u003c/span\u003e\u003c/sup\u003e. We found that the number of opportunities for cross-fertilisation (i.e. total number of spawning days) dropped with warmer temperatures and when UVR was blocked. Similarly, we found that spawning synchrony, determined with the Marquis synchrony index, also dropped in a warmer temperature regimen and when UVR was blocked. Higher synchrony occurred in conditions that yielded a higher number of spawning days, and synchrony dropped when conditions yielded a drop in number of spawning days. This relationship can happen when the number and proportion of corals involved in spawning is high on each day \u003csup\u003e\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e73\u003c/span\u003e\u003c/sup\u003e. Indeed, the higher the synchrony and the more opportunities for a high proportion of the coral population to spawn on the same day, the higher the chances of reproductive success on the reef \u003csup\u003e\u003cspan citationid=\"CR91\" class=\"CitationRef\"\u003e91\u003c/span\u003e\u003c/sup\u003e. The opposite trend (i.e. high number of spawning days related to low synchrony) was recently suggested to occur in coral communities in Eilat, northern Red Sea \u003csup\u003e\u003cspan citationid=\"CR92\" class=\"CitationRef\"\u003e92\u003c/span\u003e\u003c/sup\u003e, but the authors did not quantify synchrony directly and instead, qualitatively inferred synchrony from other reproductive metrics, without taking into account the proportion of corals that spawned in the population, without which synchrony cannot be determined \u003csup\u003e\u003cspan citationid=\"CR93\" class=\"CitationRef\"\u003e93\u003c/span\u003e\u003c/sup\u003e. In our case, in Hawai\u0026lsquo;i, we found that an increase in temperature yielded fewer spawning days and a drop in spawning synchrony. Oceans around the globe have been warming steadily since the 1970s \u003csup\u003e\u003cspan citationid=\"CR94\" class=\"CitationRef\"\u003e94\u003c/span\u003e,\u003cspan citationid=\"CR95\" class=\"CitationRef\"\u003e95\u003c/span\u003e\u003c/sup\u003e and are likely to continue warming in the next decades \u003csup\u003e\u003cspan citationid=\"CR96\" class=\"CitationRef\"\u003e96\u003c/span\u003e\u003c/sup\u003e, potentially affecting spawning synchrony throughout coral populations globally in the coming years. We found that spawning synchrony was also lower when UVR was blocked. Corals are believed to follow lunar cues to determine the days of spawning, which involves detecting low levels of blue light, which is adjacent to the ultraviolet spectrum \u003csup\u003e\u003cspan additionalcitationids=\"CR98\" citationid=\"CR97\" class=\"CitationRef\"\u003e97\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR99\" class=\"CitationRef\"\u003e99\u003c/span\u003e\u003c/sup\u003e. Blocking UVR in half of our treatments may have affected those corals\u0026rsquo; ability to detect the lunar cues in the blue range, which corals use to time their days of spawning. It is also possible that the lunar cues needed for spawning synchrony may overlap with the longer wavelengths of the ultraviolet range.\u003c/p\u003e \u003cp\u003eBoth warmer temperature regimens and ambient UVR caused a proportion of corals to start spawning a month earlier. By shifting the onset of spawning to an earlier month, these corals can spawn in better thermal conditions, showing potential for a favourable adaptation to warming conditions. A similar shift in the month of spawning has been reported in \u003cem\u003eAcropora japonica\u003c/em\u003e (but not in \u003cem\u003eA. hyacinthus\u003c/em\u003e), in \u003cem\u003eFavites pentagona\u003c/em\u003e, and in \u003cem\u003ePlatygyra contorta\u003c/em\u003e in Japan, where spawning occurred a month earlier when seawater temperatures were higher than average during the last three months of gametogenesis \u003csup\u003e\u003cspan citationid=\"CR100\" class=\"CitationRef\"\u003e100\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eIn addition to a month shift in the onset of spawning, we found that warmer temperatures caused a shift in the time of day that spawning begins, with corals exposed to higher temperatures spawning 80 min earlier on average. Most scleractinian corals spawn at night, in the hours following sunset, but \u003cem\u003eL. scutaria\u003c/em\u003e spawns in the late afternoon, presumably not using the sunset as a proximate cue for the time of spawning as night-spawning corals do \u003csup\u003e\u003cspan additionalcitationids=\"CR102\" citationid=\"CR101\" class=\"CitationRef\"\u003e101\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR103\" class=\"CitationRef\"\u003e103\u003c/span\u003e\u003c/sup\u003e. While adapting to warming temperature by advancing the onset of spawning to an earlier month is advantageous in avoiding hotter water temperatures, spawning earlier in the afternoon will cause gametes to be released at a time of the day when the water is warmer and insolation is stronger. Hotter- than-normal temperatures at the time of gamete release can reduce fertilisation success, cause abnormalities in developing larvae, and reduce larval survival \u003csup\u003e\u003cspan citationid=\"CR104\" class=\"CitationRef\"\u003e104\u003c/span\u003e,\u003cspan citationid=\"CR105\" class=\"CitationRef\"\u003e105\u003c/span\u003e\u003c/sup\u003e. In addition, stronger insolation can lead to DNA damage to the gametes and developing larvae due to stronger ultraviolet radiation \u003csup\u003e\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e48\u003c/span\u003e,\u003cspan citationid=\"CR106\" class=\"CitationRef\"\u003e106\u003c/span\u003e,\u003cspan citationid=\"CR107\" class=\"CitationRef\"\u003e107\u003c/span\u003e\u003c/sup\u003e. While this effect is alarming, we found that the shift in spawning to earlier in the afternoon caused by higher water temperature can be reset in just three days, as we accidentally found out when we had to evacuate all corals to a safer tank due to Hurricane Lane in August 2018. While the exact mechanisms by which the fungiid corals synchronise their spawning to the same time of day remain unknown, we found that water temperature played a significant role, either as a direct cue, or through disrupting the mechanisms responsible for determining the timing.\u003c/p\u003e \u003cp\u003eFertilisation success is highly dependent on a sufficiently high concentration of motile sperm \u003csup\u003e\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e,\u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e75\u003c/span\u003e\u003c/sup\u003e. Once above a minimum ratio threshold of 5\u0026times;10\u003csup\u003e3\u003c/sup\u003e sperm per egg for the coral \u003cem\u003eL. scutaria\u003c/em\u003e \u003csup\u003e\u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e75\u003c/span\u003e\u003c/sup\u003e, fertilisation is generally high, which is likely why we obtained high fertilisation success in all treatments. Higher temperature caused a drop in fertilisation success with the lowest fertilisation rates observed at warmer temperature, low PAR and ambient UVR. A few studies have investigated the effect of short-term increased temperature during the stages of fertilisation success and larval development in corals and have found that an increase in temperature during these stages tended to accelerate the duration of larval development \u003csup\u003e\u003cspan citationid=\"CR104\" class=\"CitationRef\"\u003e104\u003c/span\u003e\u003c/sup\u003e but did not necessarily cause a drop in fertilisation success, except in \u003cem\u003eAcropora millepora\u003c/em\u003e \u003csup\u003e\u003cspan citationid=\"CR104\" class=\"CitationRef\"\u003e104\u003c/span\u003e\u003c/sup\u003e. In the coral \u003cem\u003eA. tenuis\u003c/em\u003e, the sperm concentration threshold necessary for successful fertilisation was found to be possibly higher at increased temperatures, requiring approximately a 6- to 8-fold higher sperm concentration at 3\u0026deg;C above ambient temperatures in the coral \u003cem\u003eA. tenuis\u003c/em\u003e \u003csup\u003e\u003cspan citationid=\"CR108\" class=\"CitationRef\"\u003e108\u003c/span\u003e\u003c/sup\u003e. However, the authors did not evaluate sperm motility, so the need for increased sperm concentration could simply have been to compensate for lower sperm motility at higher temperature to obtain similar fertilisation success rates. Following bleaching events, drops in fertilisation have been apparent in several coral species \u003csup\u003e\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e,\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e\u003c/sup\u003e, but many confounding effects other than temperature could have been involved. The present study is the first that tests the independent effect of temperature over a period of several months, here encompassing the full gametogenesis cycle, on reproductive success. Our results confirm that the effects of temperature and other coral bleaching-related environmental stressors such as solar radiation on fertilisation success can remain minimal as long as sperm concentration is high. Some temperature effect was noted, but we would suggest further studies using lower concentrations of motile sperm to identify the limits of fertilisation success under different levels of environmental stress.\u003c/p\u003e \u003cp\u003eUnlike fertilisation success, sperm motility dropped at high PAR and was not affected by temperature. The lack of correlation with temperature suggests that although some sperm motility is important for fertilisation success, here other factors may be involved. For example, we found the strongest effect on egg volume to be temperature, with a drop in egg size at warmer temperatures. The smaller eggs might have been the cause of the reduced fertilisation success in the higher temperature treatments. Sperm motility has been overall low since two consecutive bleaching events in Hawaiʻi in 2014 and 2015 \u003csup\u003e33\u003c/sup\u003e. Loss of sperm motility is paired with a loss in sperm mitochondrial membrane potential (MMP) in humans \u003csup\u003e\u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e109\u003c/span\u003e,\u003cspan citationid=\"CR110\" class=\"CitationRef\"\u003e110\u003c/span\u003e\u003c/sup\u003e and bovines \u003csup\u003e\u003cspan citationid=\"CR111\" class=\"CitationRef\"\u003e111\u003c/span\u003e\u003c/sup\u003e, but also in marine invertebrates such as sea urchins \u003csup\u003e\u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e76\u003c/span\u003e,\u003cspan citationid=\"CR112\" class=\"CitationRef\"\u003e112\u003c/span\u003e\u003c/sup\u003e and in some coral species \u003csup\u003e\u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e56\u003c/span\u003e\u003c/sup\u003e. Indeed, a high proportion of high MMP reflects the process of electron transport and oxidative phosphorylation, the driving force behind ATP production and therefore sperm motility. However, this relationship was not found in sperm from marine ascidians or mussels; loss of sperm motility was instead correlated to reactive oxygen species levels and plasma membrane lipid peroxidation \u003csup\u003e\u003cspan citationid=\"CR111\" class=\"CitationRef\"\u003e111\u003c/span\u003e\u003c/sup\u003e. Similarly, in sperm from the coral \u003cem\u003eL. scutaria\u003c/em\u003e, we found no relation between MMP and sperm motility. Here, the cause of the loss of sperm motility is therefore elsewhere. That sperm motility was diminished at high PAR suggests that the stress that primarily drove sperm motility here likely occurred at the level of the symbiont, the photosynthetic partner in the symbiosis, during spermatogenesis. Several studies report negative effects from UVR or combined UVR and PAR on the sperm motility of corals \u003csup\u003e\u003cspan citationid=\"CR113\" class=\"CitationRef\"\u003e113\u003c/span\u003e\u003c/sup\u003e and other marine invertebrates \u003csup\u003e\u003cspan citationid=\"CR114\" class=\"CitationRef\"\u003e114\u003c/span\u003e,\u003cspan citationid=\"CR115\" class=\"CitationRef\"\u003e115\u003c/span\u003e\u003c/sup\u003e, but few from PAR alone. In a study comparing DNA damage, a sign of advanced cell apoptosis, in coral larvae with and without symbionts when exposed to direct insolation (high PAR and high UVR were coupled), DNA damage was higher in larvae with symbionts than in larvae without symbionts, indicating that the symbionts were the source of oxidative stress \u003csup\u003e\u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e116\u003c/span\u003e\u003c/sup\u003e. To understand how oxidative stress in the symbionts led to a decrease in sperm motility, further work testing gene expression regulatory mechanisms is needed, possibly with high resolution imaging to identify any morphological anomalies. Testing the direct effects of reactive oxygen species, the toxic compound released during photo-oxidative stress, on sperm cells, during their development or after their release, might also provide valuable answers.\u003c/p\u003e \u003cp\u003eThe volume of the eggs released by female \u003cem\u003eL. scutaria\u003c/em\u003e individuals was reduced at warmer temperatures, but it also dropped at higher PAR and was lower in the first month of spawning (i.e. June). A similar temperature effect was found in the coral \u003cem\u003eAcropora digitifera\u003c/em\u003e in Okinawa when exposed to temperature regimens 2\u0026deg;C above ambient temperatures over several weeks prior to spawning \u003csup\u003e\u003cspan citationid=\"CR117\" class=\"CitationRef\"\u003e117\u003c/span\u003e\u003c/sup\u003e. Eggs are mostly composed of lipids, which will act as energy reserves for the developing larva. To build up enough lipids to produce larger eggs, sufficient resources need to be available. These are provided by the photosynthetic symbionts as part of their symbiotic relationship with their coral host, which relies on the symbionts being healthy and abundant. In this study we found that both temperature and PAR caused corals to pale, which indicates that the symbionts were at the very least less abundant and likely not able to provide as many nutrients to their coral host as their counterparts in the lower temperature and PAR treatments.\u003c/p\u003e \u003cp\u003eAlthough warmer temperatures, PAR, and UVR all caused paling of corals, coral growth was affected only by the warmer temperature treatments that represent recent temperature observations on reefs in Kāneʻohe Bay (based on data 2014\u0026ndash;2019). Previous work in Kāneʻohe Bay has shown that the optimal temperature for coral calcification, including for \u003cem\u003eL. scutaria\u003c/em\u003e, is 25.9\u0026deg;C and that coral growth drops when above that threshold \u003csup\u003e\u003cspan citationid=\"CR118\" class=\"CitationRef\"\u003e118\u003c/span\u003e\u003c/sup\u003e. Our results confirm these earlier results but alarmingly suggest that coral growth might be already dropping throughout Kāneʻohe Bay due to ocean warming. Elsewhere, reductions in coral growth linked with warming ocean temperatures have already been detected in the Red Sea \u003csup\u003e\u003cspan citationid=\"CR119\" class=\"CitationRef\"\u003e119\u003c/span\u003e\u003c/sup\u003e, on the Great Barrier Reef \u003csup\u003e\u003cspan citationid=\"CR120\" class=\"CitationRef\"\u003e120\u003c/span\u003e\u003c/sup\u003e, in the Andaman Sea \u003csup\u003e\u003cspan citationid=\"CR121\" class=\"CitationRef\"\u003e121\u003c/span\u003e,\u003cspan citationid=\"CR122\" class=\"CitationRef\"\u003e122\u003c/span\u003e\u003c/sup\u003e, and in the South China Sea \u003csup\u003e\u003cspan citationid=\"CR122\" class=\"CitationRef\"\u003e122\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eThe physiological effects of global climate change on coral reproduction are numerous and complex. However, the bottom line is that without robust reproduction, corals may not be able to adapt to changing ocean conditions. We show that warming ocean temperatures and high solar radiation both negatively affect the reproductive physiology of the mushroom coral \u003cem\u003eL. scutaria\u003c/em\u003e, but they may do so through different cellular pathways. Oceans are predicted to continue warming in the decades to come, which will likely cause a further reduction in coral spawning synchrony, disrupt the timing of spawning, cause a further drop in fertilisation success and in egg volume, and slow coral growth. To manage warming ocean temperatures will take a global effort and strong political will and action, but that effort is necessary to prevent the loss of coral reefs and the vital ecosystems services that they provide \u003csup\u003e\u003cspan citationid=\"CR123\" class=\"CitationRef\"\u003e123\u003c/span\u003e\u003c/sup\u003e.\u003c/p\u003e \u003cp\u003eWhile high levels of PAR are likely to continue to affect the reproductive physiology of corals in the coming decades, artificially controlling PAR levels may be an effective option to reduce damage to sperm and eggs, and to mitigate bleaching effects under thermal stress. Shading corals has been tested for a variety of coral species, showing promising results in reducing coral bleaching and decreasing effects on overall fitness \u003csup\u003e\u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e71\u003c/span\u003e\u003c/sup\u003e. Our results suggest that it could also prevent damage to coral gametes, thus reducing the risk of reproductive failure. Shading can be managed at a local level, targeting coral reefs of special interest, as sole intervention or in conjunction with other interventions such as enhancing coral recruitment or implementing assisted gene flow \u003csup\u003e\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e,\u003cspan citationid=\"CR124\" class=\"CitationRef\"\u003e124\u003c/span\u003e,\u003cspan citationid=\"CR125\" class=\"CitationRef\"\u003e125\u003c/span\u003e\u003c/sup\u003e. Finally, high levels of ultraviolet radiation are known to cause cellular damage in many organisms but lower levels of UVR may play an important functional role. Here, we show that completely blocking UVR can impair lunar cycle\u0026ndash;related cues, on which the corals rely for determining the timing of spawning and maintaining spawning synchrony.\u003c/p\u003e \u003cp\u003eThe coming decades will be challenging for coral reefs around the world, but one of the key steps to conserving reef-building corals, will be to ensure that reproduction is maintained. This will require global, annual monitoring of coral reproduction. If reproductive issues are anticipated, measures can be put in place to aid reproductive events on a regional scale through mitigating environmental stress, e.g., by shading reefs or specific corals. On a longer time-scale, global pressures from climate change will need to be addressed for oceans to return to thermal conditions more suitable for the world\u0026rsquo;s coral reefs to thrive again.\u003c/p\u003e "},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eData Availability Statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe data supporting the findings of this paper are available in the article and Supplementary Information.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis research was supported by funds from the Smithsonian Institution, the Smithsonian Conservation Biology Institute,\u0026nbsp;the Hawaiʻi Institute of Marine Biology, the Paul M. Angell Family Foundation, the Roddenberry Foundation, the Seaver Institute, the William H. Donner Foundation, the Barrett Family Foundation, the Skippy Frank Foundation, the Compton Foundation, the Cedar Hill Foundation, the Anela Kolohe Foundation, and the Smithsonian Women\u0026rsquo;s Committee. The authors would like to thank Katherine Hardy, Brock Wetzlich, and Ned Busch, for assisting with spawning observations and gamete collection.\u0026nbsp;This manuscript was given an HIMB contribution # XXX.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eJB, JD, NH, CL, EMH, and MH conceived the ideas and designed the methodology. JB, JD, NH, CL, EMH, MQ, and MH collected the data. JB and MH analysed the data and wrote a first draft of the manuscript. All authors provided critical feedback to the manuscript and approved the submitted version.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAdditional Information\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare no competing interests.\u0026nbsp;\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003e\u003cspan\u003eMoberg, F. \u0026amp; Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. \u003cstrong\u003e29\u003c/strong\u003e, 215\u0026ndash;233 (1999).\u003c/span\u003e\u003c/li\u003e\n \u003cli\u003e\u003cspan\u003ePlaisance, L., Caley, M. J., Brainard, R. E. \u0026amp; Knowlton, N. The Diversity of Coral Reefs: What Are We Missing? 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Coral Reefs \u003cstrong\u003e41\u003c/strong\u003e, 455\u0026ndash;462 (2022).\u003c/span\u003e\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Broadcast Spawning, Climate Change, Computer Assisted Sperm Analysis, Fungia scutaria, Photosynthetically Active Radiation, Seawater Temperature, Spawning Synchrony, Ultraviolet Radiation","lastPublishedDoi":"10.21203/rs.3.rs-1864235/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-1864235/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eCoral reefs worldwide are at risk due to climate change. Coral bleaching is becoming increasingly common and corals that survive bleaching events can suffer from temporary reproductive failure for several years. While water temperature is a key driver in causing coral bleaching, other environmental factors are involved, such as solar radiation. We investigated the individual and combined effects of temperature, photosynthetically active radiation (PAR), and ultraviolet radiation (UVR) on the spawning patterns and reproductive physiology of the Hawaiʻian mushroom coral \u003cem\u003eLobactis scutaria\u003c/em\u003e, using long-term experiments in aquaria. We examined effects on spawning timing, fertilisation success, and gamete physiology. Both warmer temperatures and filtering UVR altered the timing of spawning. Warmer temperatures caused a drop in fertilisation success. Warmer temperatures and higher PAR both negatively affected sperm and egg physiology. Thermal stress from global climate change will need to be adequately addressed to ensure the survival of reef-building corals in their natural environment throughout the next century and beyond. Until then, reproduction is likely to be increasingly impaired. On a regional scale, some damage related to photo-oxidative stress may be partially mitigated through shading reefs or specific corals, to reduce bleaching, minimise the loss of coral fitness, and maintain coral reproduction.\u0026nbsp;\u003c/p\u003e","manuscriptTitle":"Coral Reproduction in a Changing Climate","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2022-07-27 19:52:25","doi":"10.21203/rs.3.rs-1864235/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Major revision","date":"2022-08-29T08:18:27+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2022-08-15T22:25:52+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"ac090acc-778c-4161-8aff-6002be1ceec9","date":"2022-07-26T20:10:47+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2022-07-22T08:17:13+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2022-07-21T13:50:13+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2022-07-21T07:36:23+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2022-07-21T07:33:34+00:00","index":"","fulltext":""},{"type":"submitted","content":"Scientific Reports","date":"2022-07-16T10:12:38+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"d7028e94-1116-4ac5-92de-f02e3e5c714a","owner":[],"postedDate":"July 27th, 2022","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2023-10-16T18:15:55+00:00","versionOfRecord":{"articleIdentity":"rs-1864235","link":"https://doi.org/10.1038/s41598-022-27207-6","journal":{"identity":"scientific-reports","isVorOnly":false,"title":"Scientific Reports"},"publishedOn":"2023-01-05 18:13:58","publishedOnDateReadable":"January 5th, 2023"},"versionCreatedAt":"2022-07-27 19:52:25","video":"","vorDoi":"10.1038/s41598-022-27207-6","vorDoiUrl":"https://doi.org/10.1038/s41598-022-27207-6","workflowStages":[]},"version":"v1","identity":"rs-1864235","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-1864235","identity":"rs-1864235","version":["v1"]},"buildId":"FbvkV6FR0MCFSLy54lSbu","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}