Dissecting coral recovery: Bleaching reduces reproductive output in Acropora millepora

Dissecting coral recovery: Bleaching reduces reproductive output in Acropora millepora | 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 Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Dissecting coral recovery: Bleaching reduces reproductive output in Acropora millepora Nico D Briggs, Cathie A Page, Christine Giuliano, Cinzia Alessi, and 3 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3346366/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 20 Mar, 2024 Read the published version in Coral Reefs → Version 1 posted You are reading this latest preprint version Abstract Increasingly frequent and severe bleaching events driven by climate change are decreasing coral populations worldwide. Recovery of these populations relies on reproduction by the survivors of such events including local and upstream larval sources. Yet, corals that survive bleaching may be impaired by sublethal effects that suppress reproduction, reducing larval input to reefs, and consequently impeding recovery. We investigated the impact of the 2020 mass-bleaching event on Acropora millepora reproduction on inshore, turbid reefs in Woppaburra sea Country (the Keppel Islands), to improve our understanding of the effects of bleaching on coral populations. A. millepora experienced high bleaching incidence but low mortality across the island group during this event and thus constituted an ideal population to investigate potential sublethal effects on reproductive output. Six months after the heat wave, and just prior to spawning, we collected, decalcified, and dissected samples from 94 tagged A. millepora colonies with a known 2020 bleaching response, to investigate the relationships between stress severity and reproduction. Despite having regained their pigmentation, we detected a significant reduction in fecundity in colonies that had bleached severely. Considering the impact of the bleaching event on the coral population sampled (i.e. mortality, bleaching severity and colony size), coupled with reductions in fecundity, we estimated a total decrease in population-level reproductive output of 21%. These results suggest that reduced reproductive output may impact recovery of coral populations following bleaching and should be considered alongside traditional estimates from coral mortality. Marine and Freshwater Ecology Fecundity egg size bleaching severity sublethal effects climate change ocean warming Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction Coral reefs support key ecological functions and ecosystem services that are important for humans (Sheppard et al. 2005 , Worm et al. 2006 , Cinner et al. 2016 ). However, increasingly frequent climate-change driven disturbance events, including regional scale mass-coral bleaching, have negatively affected coral reefs globally and are challenging the ecosystem’s recovery potential (Hughes et al. 2017 , 2018a , Sully et al. 2019 ). An estimated 50% of coral cover worldwide has been lost since the 1950s and a downward trajectory is predicted to continue throughout the 21st century (van Hooidonk et al. 2016 , Eddy et al. 2021 ). Consequently, the capacity for coral reefs to support critical ecosystem services is declining (Hughes et al. 2018b , Hughes et al. 2019 , Eddy et al. 2021 ), and the future value of reef systems will depend on their persistence under future climate-change emission scenarios (Hoegh-Guldberg et al. 2007 , Chen et al. 2015). Recovery and persistence of reefs after disturbances is driven by the growth of surviving colonies (van Oppen et al. 2015 ) and by larval recruitment from sexual reproduction (Glynn et al. 2012 ). Larval supply comes from both mass-spawning events (i.e., the synchronous release of gametes by spawning corals at particular times of the year), and from brooding corals, which experience internal fertilization and then release fully developed larvae (Sakai et al. 2020 ). In both cases, reproduction is energetically costly, requiring a build-up of energy reserves prior to spawning (Leuzinger et al. 2003 , Anthony et al. 2007 ). Coral eggs are comprised of proteins, carbohydrates, and lipids, which aid in embryo floatation and provide an energy source for the developing larvae (Harii et al. 2007 , 2010 ). The accumulation of lipids and other macromolecules is directly impacted by the breakdown of the coral host-symbiont relationship and the resulting decline in nutrition from the symbiont to the coral host (Conlan et al. 2020 , Rodrigues and Padilla-Gamiño 2022 ). Energy use by corals is also altered during bleaching and can lead to physiological trade-offs, including the differential partitioning of energy between gamete production and colony maintenance (Rodrigues and Padilla-Gamiño 2022 ). Due to the annual reproductive cycle in many coral species, oocyte maturation and/or spawning often coincides with summer heat-stress (Randall et al. 2020 ), Shikina and Chang 2016 ), increasing the potential for bleaching to impact reproductive output. Therefore, understanding how bleaching events influence the production of coral gametes, and subsequent supply of larvae to degraded reefs, can inform our understanding of the recovery capacity of coral populations and communities. To date, three primary effects of heat-stress on coral reproduction have been documented and include, in decreasing order of severity: (i) complete failure of gametogenesis; (ii) a decrease in fecundity; and (iii) a decline in gamete viability. Firstly, complete failure to produce gametes is the most well-documented sublethal impact of bleaching on coral reproduction (Ward et al. 2002 , Levitan et al. 2014 ) and has been recorded during heat-stress conditions even when colonies showed no visible signs of bleaching (Rodriguez-Troncoso et al. 2011). Secondly, a decline in metrics of reproductive output such as egg size and fecundity has been observed in response to bleaching (Michalek-Wagner and Willis 2001 , Baird and Marshall 2002 , Ward et al. 2002 , Cox 2007 ). For example, Jones and Berkelmans ( 2011 ) found that bleached Acropora millepora colonies produced smaller and 50% fewer eggs, and that the proportion of colonies within the population that were reproductive had declined. Thirdly, some studies have demonstrated an effect of bleaching on gamete and larval viability. For example, Hagedorn et al. ( 2016 ) documented a decline in sperm motility and fertilization rates following bleaching, while an increase in developmental abnormalities and a decline in larval survival in response to direct heat stress has been observed (Randall and Szmant 2009 , Lenz et al. 2021 ). While most studies examine the immediate impacts of heat stress or bleaching on reproduction, how long these effects persist following heat stress and colony recovery remains unclear. Furthermore, variability in the persistence of these sublethal effects has been noted across species, geographic regions and environmental regimes. Therefore, continuing to investigate the potential long-term sub-lethal impacts of bleaching on species and reefs is critically important for predicting coral responses to future climate warming. Severe and widespread bleaching occurred within Woppaburra sea Country (the Keppel Islands, southern inshore Great Barrier Reef (GBR)) in March - April 2020. Although mortality was low (Page et al. 2023 ), it was unknown whether the surviving corals suffered any impacts to reproduction in the spawning season following bleaching. Furthermore, individual bleaching responses were highly variable, and the relationship between bleaching severity and post-bleaching reproductive output is not well documented (Leinbach et al. 2021 ). To address these knowledge gaps, we tagged Acropora millepora colonies during bleaching and tracked their fates over six months. Colonies that spanned the full spectrum of bleaching phenotypes, from none to catastrophic, were then sampled, decalcified, and dissected to address the following research questions: (i) what is the relationship between bleaching severity and fecundity? (ii) how does post-bleaching fecundity compare with historical baselines? (iii) are bleaching severity, colony size, and coral mortality related? Methods Site selection, sample collection and decalcification This study was conducted on fringing reefs in the Keppel Islands of the southern inshore GBR. Four sites were selected across the Island group: Great Keppel Island (GKI, 23.1030° S 150.5740° E), North Keppel Island (NKI, 23.0738° S, 150.8987° E), Halfway Island (HI, 23.1984° S, 150.9718° E), and Pumpkin Island (PI, 23.0927° S, 150.9011° E) (Fig. 1 ) and were at 1 to 5 m depth below lowest astronomical tide (LAT). Acropora millepora is a corymbose species common across Woppaburra sea Country where it has been extensively studied (Jones and Berkelmans 2011 ). Between 18 and 21 April 2020, at the height of the heatwave induced bleaching, 350 adult A. millepora colonies (~ 10–75 cm maximum diameter, average = 30 cm) were haphazardly tagged across sites, to capture a wide range of bleaching phenotypes within the populations. Colonies were tagged at each of NKI (n = 100), PI (n = 101), HI (n = 99), and GKI (n = 50). During tagging, colonies were assigned an in situ ordinal bleaching score that ranged from 1 to 6, based on the CoralWatch Coral Health Chart (Siebeck et al. 2006 ) and were photographed (Fig. 1 ). Between 7 and 17 October 2020, approximately 1 month prior to the predicted coral spawning (realized on 9 Nov 2020 for colonies from the population (C. Randall personal observation)) and approximately 6 months following the height of bleaching, 311 tagged colonies were re-surveyed and the following data were recorded: (i) mortality status (dead or alive), (ii) percentage of live tissue remaining in intervals of 10% (i.e. 10–100% live tissue), (iii) maximum diameter (cm), (iv) maximum perpendicular diameter (cm), and (v) bleaching score (1–6), as described above. Colonies that were not sampled at the second time point (n = 39) were excluded from analysis. Estimated surface area of live tissue \(\left(SA\right)\) was calculated for each colony from the maximum diameter ( \(a\) ) and the maximum perpendicular diameter ( \(b\) ), both of which were recorded across a horizontal plane by a diver, using Eq. 1: \(SA = \pi \left(\frac{1}{2}a\right)\left(\frac{1}{2}b\right)\) .Mean colony diameter was also calculated from \(a\) and \(b\) . During resurvey, three replicate branches were sampled from the central area of each colony to avoid the sterile zone found at the outer margins of Acropora colonies (Wallace 1985 , Randall et al. 2021 ). Branches were collected using a small chisel or knife and were placed in pre-labeled sample bags with seawater. Immediately post dive, coral samples were transferred to a solution of 10% formaldehyde in 1 µm filtered seawater (FSW) (hereafter ‘formalin’). Samples were then transferred into 3% hydrochloric acid (HCl) in FSW solution for decalcification, and additional 3% HCl was added over a few days to replenish the weak acid until complete decalcification of the branches had occurred (decalcification durations varied from 3 to 10 days). Decalcified tissue samples were rinsed in FSW and stored in fresh formalin until dissection. Sample dissection Decalcified samples from a total of 94 colonies were dissected to assess fecundity. Colonies were systematically chosen for dissection to ensure an even representation across the range of bleaching phenotypes and, where possible, sites (Fig. 2 b). Branches were dissected under a Lecia M60 Stereomicroscope at 20x − 40x magnification. Measurements were taken at 25x magnification from live image (5mp digital C-mount camera) within ToupView software. Maximum branch length was measured with digital calipers, and then a longitudinal section was cut through the middle of the branch, which was suspended in FSW in a wax dish, using a scalpel (Fig. 3 a). The length of the sterile zone— the tip of Acropora branches where the newest growth lacks gonads (Wallace 1985 )—was clearly visible from the longitudinal section and measured from the apical polyp tip to the nearest visibly fecund polyp (Fig. 3 a). Ten polyps were haphazardly selected from near the base of the branch, with the branch interior facing downward, in order to minimize bias in selecting polyps that had visible eggs; polyps were then removed with forceps and dissected as per Wallace 1985 (Fig. 3 b). Very small polyps were avoided, although smaller than average polyps were sometimes selected as a result of the haphazard process and, in most instances, were observed to be reproductively mature. The number of polyps (out of 10) that had successfully produced oocytes was recorded. Then, the number of oocytes within each polyp was counted, and for each of the first three polyps containing eggs, the maximum diameter \(\left(d\right)\) was recorded for each egg observed. Egg volume ( \(V\) ) was then estimated using Eq. 2: \(V=\frac{4}{3}\pi {\left(\frac{d}{2}\right)}^{3}\) , assuming a sphere. Statistical Analysis All statistical analyses were completed in R (R Core Team, 2022 ). Generalized linear mixed effect models (GLMM) utilizing a template model builder (Brooks et al. 2017 ) were used to model reproductive output. Models were created to test for the additive effects of bleaching score, site, and mean colony diameter on three reproductive metrics: (1) egg size, (2) number of eggs per polyp, and (3) number of eggs per fecund polyp. Replicate branch within colony, and colony within site were treated as nested random effects in the model of egg size. In the models of egg numbers, only colony within site was treated as a nested random effect due to a lack of convergence in the full model. All response variables (egg size, number of eggs per polyp, and number of eggs per fecund polyp) were modelled with a Gaussian distribution. A null model was formulated using only random effects and model selection was undertaken by comparing models with each combination of predictors against the null model, using second-order Akaike Information Criterion (AICc) in the MuMIn package (Bartoń 2013). Analysis of Variance (ANOVA) was used to statistically compare models and validate model selection. Based on this model selection method, site and mean diameter were not included in the final models of number of eggs per polyp and number of eggs per fecund polyp. Model assumptions were assessed and validated using DHARMa residual analysis (Hartig 2021 ) and results were visualized using ‘ggplot2’ (Wickham 2016 ). Colony size does not appear to determine reproductive output of each polyp in A. millepora once coral maturation is reached at approximately 15 cm in diameter (Hall and Hughes 1996 , Baria et al. 2012 ). Therefore, two colonies from NKI that were less than 15 cm diameter were excluded from the analysis. Samples from HI were also removed from the site-specific models due to a comparatively small sample size (HI n = 4, PI n = 29, NKI n = 34, GKI n = 27). Therefore, a total of 88 colonies were included in the models testing site-level variation, and 92 colonies were included in fecundity models. To investigate the relationship between bleaching score and colony survival, a logistic regression with a binomial distribution and a logit link function was modelled using ‘glm’ from the ‘stats’ package and diagnostics were checked as described above (R Core Team, 2022 ). Historical Data Three years of historical A. millepora fecundity data from the Keppel Islands were used to establish a baseline of reproductive output prior to recent bleaching. Firstly, Tan et al. ( 2016 ) measured the number of eggs per polyp from haphazardly selected A. millepora colonies in a manner comparable to this study, in 2009 and 2010, prior to the 2016 and 2017 bleaching events. Secondly, following the sampling methods described above, a single branch from 49 haphazardly sampled colonies from 10 sites across the Keppel Islands in October 2019 (6 months before bleaching) were dissected, 12–19 days prior to 2019 spawning. To determine whether reproductive output in 2020 differed from these baselines, we modelled the number of eggs per polyp against year using a general linear model with a Gaussian distribution, as described above. Estimate of population level reduction in fecundity Based on the results of this study, a population level fecundity reduction was estimated from the bleaching data that were collected from all 310 colonies surveyed during bleaching in April 2020. Firstly, a hypothetical population-level fecundity potential was calculated, in the absence of bleaching. To do this, we first assumed a sterile zone of length 7.3 mm around the colony perimeter as per the mean sterile zone measured from all replicates. We then re-calculated the maximum fecund diameter ( \(a\) ) and maximum fecund perpendicular diameter \(\left(b\right)\) for each colony by subtracting 14.6 mm (7.3 mm on each side) from each metric and used those values to calculate a ‘fecund SA’ in cm 2 for each colony using Eq. 1. The total number of fecund polyps per colony was then estimated by multiplying the fecund SA of planar area measured by diameter (in cm 2 ) by the average density of polyps in Acropora millepora (87 polyps cm − 2 ; Hall and Hughes 1996 ). From this, the modelled number of eggs per polyp, assuming no bleaching (score = 6; 7.47 eggs per polyp), was multiplied by the number of reproductive polyps per colony, to create a baseline assumption of a colony’s potential reproductive output, if healthy. Then, to account for bleaching and partial mortality, the number of fecund polyps for each colony was reduced by the % reduction in egg number estimated for that colony’s bleaching score and then reduced by the % partial mortality observed, to estimate a realized reproductive output following bleaching. For colonies that suffered complete mortality, realized reproductive output was zero. Finally, the percentage reduction between the hypothetical reproductive output and the estimated realized reproductive output for all colonies combined was calculated, providing an estimate of the impact of the 2020 bleaching event on population-level fecundity. We note that this method assumes a planar SA and thus likely underestimates the colony-level reproductive potential, although the estimated percentage reduction should scale proportionally. Comparison of diver assessed and photo-surveyed bleaching scores To assess whether field images of colonies could be used to accurately identify bleaching severity, bleaching scores were estimated from images taken in April 2020 using Coral Point Count with Excel Extensions (CPCe), from 10 randomly placed points overlaid on each colony, excluding those points that fell on the growing tips of the colonies, which are naturally paler than the surrounding colony (Kohler et al. 2006). The relationship between in situ diver assessed and ex situ photo-surveyed bleaching scores was tested using a Pearson’s correlation coefficient with the function cor.test in base R (R Core Team 2022 ). Results Of the colonies phenotyped during the height of bleaching (April 2020), 61% had a severe bleaching response (category = 2, n = 214) while 15% had a catastrophic response (category = 1, n = 53), together accounting for 76% of all colonies scored (Fig. 2 a). Only 4.5% of colonies did not visually bleach (category = 6, n = 16). Whole-colony mortality was highest at PI (17%, n = 16) while no whole-colony mortality was observed at NKI (SI Table 1 , Page et al. 2023 ). The likelihood of survival significantly increased as a function of bleaching score (GLM: z = 3.437, p < 0.001) (Fig. 2 d); only ‘catastrophically’ and ‘severely’ bleached colonies (scores of 1 and 2, respectively) suffered whole-colony mortality (2.9% in score 1 (n = 9) and 3.5% in score 2 (n = 11), which equated to an overall mortality of 6.5% (n = 20). Partial mortality ranged from 10–90%, but occurred rarely (incidence of 2%), and only in severely bleached colonies (score of 2, n = 6). As colony size increased, the bleaching response became more severe (Fig. 2 c). Nearly all colonies had recovered by October, with an average score of 5 (‘negligible’ bleaching) at all sites at that time, with only two colonies retaining a ‘mild’ level of bleaching (score 3, n = 2). Egg Number Polyp fecundity (number of eggs per polyp and number of eggs per fecund polyp) significantly differed by bleaching score, but not by site (Table 1 , Fig. 4 c, d). Egg output per polyp decreased by approximately 21% from the least bleached (7.5 eggs per polyp) to the most bleached (5.9 eggs per polyp) colonies (SE = 0.77, p = < 0.05), with similar results in the egg output per fecund polyp model (SE = 0.63, p = < 0.05) (Table 1 ). While egg output differed in the overall models between scores of 1 and 6, pairwise post-hoc Tukey tests showed no significant pairwise differences in either model. Egg Size Bleaching score was not a significant predictor of egg size, although site and colony diameter were (Fig. 4 a, b). Eggs from GKI colonies were 0.05 mm larger than eggs from NKI colonies (SE = 0.01, p < 0.0001) and 0.04 mm larger than eggs from PI colonies (SE = 0.01, p < 0.01) (Table 1 ). These size estimates equate to an approximate 10% difference in egg diameter, and a consequent 25% difference in egg volume between GKI and NKI. Table 1 Estimated marginal mean (emmean) egg size, number of eggs per polyp, and number of eggs per fecund polyp modelled against bleaching field score and site as fixed effects. Site abbreviations are as in Fig. 1 . Fecundity Metric Best Model Bleaching score/ Site emmean SE df lower.CL upper.CL Mean Egg Size Fecundity ~ Field Score + Site + Mean Diameter + (1|Sample/Rep) 1 0.53 0.008 770 0.516 0.549 2 0.54 0.011 770 0.515 0.557 3 0.54 0.026 770 0.489 0.591 4 0.56 0.017 770 0.527 0.594 5 0.54 0.010 770 0.523 0.563 6 0.55 0.013 770 0.528 0.580 Fecundity ~ Field Score + Site + Mean Diameter + (1|Sample/Rep) GKI 0.57 0.009 770 0.557 0.591 NKI 0.52 0.010 770 0.503 0.541 PI 0.54 0.009 770 0.519 0.555 Mean # of Eggs Per Polyp Fecundity ~ Field Score + (1|Sample) 1 5.9 0.402 252 5.109 6.694 2 6.04 0.497 252 5.065 7.023 3 6.59 1.251 252 4.125 9.052 4 6.29 0.819 252 4.677 7.903 5 7.08 0.511 252 6.070 8.085 6 7.47 0.653 252 6.180 8.753 Fecundity ~ Field Score + Site + (1|Sample) GKI 6.6 0.434 250 5.743 7.451 NKI 6.65 0.504 250 5.661 7.646 PI 6.46 0.450 250 5.572 7.341 Mean # of Eggs Per Fecund Polyp Fecundity ~ Field Score + (1|Sample) 1 6.22 0.330 248 5.575 6.873 2 6.73 0.419 248 5.900 7.551 3 7.11 1.025 248 5.089 9.126 4 6.57 0.671 248 5.245 7.887 5 7.16 0.419 248 6.336 7.987 6 7.68 0.535 248 6.630 8.738 Fecundity ~ Field Score + Site + (1|Sample) GKI 6.86 0.355 246 6.162 7.562 NKI 6.91 0.413 246 6.095 7.722 PI 6.97 0.373 246 6.239 7.707 Population-level fecundity Based on the estimate of fecundity for each bleaching score, combined with whole-colony and partial mortality, we estimated a 21% reduction in total oocyte output of the population six months after the 2020 bleaching event. Coral fecundity past and present Mean number of eggs per fecund polyp in 2020 did not differ from pre-bleaching baselines (Fig. 4 e). Samples from 2019 and unbleached samples in 2020 (scores of 5 and 6) had a higher mean polyp fecundity than compared to the historic baseline, but bleached colonies in 2020 (scores of 1 and 2) had a similar or lower polyp fecundity than historic baselines. Comparison of diver assessed and photo-surveyed bleaching scores Diver assessed and photo surveyed (CPCe) bleaching scores were tightly and positively correlated (t = 29.99, df = 348, p < 0.001, r = 0.85) (Fig. S1). The greatest variance in CPCe score was found for colonies with field scores of 2 and 3, while the least variance was seen for colonies at either end of the scale (scores 1 and 6). However, some colonies scored as ‘severe’ (score = 2) by divers in situ were scored as not bleached by the CPCe method, indicating the potential for some underestimation of bleaching from images (Fig. S1). Discussion Severe bleaching occurred throughout Woppaburra sea Country (the Keppel Islands) during the 2020 marine heatwave, but mortality of Acropora millepora was low (~ 6.5% this study; Page et al. 2023 ). Despite recovery by the time of coral spawning six months later, we found that heavily bleached colonies experienced a significant reduction in reproductive output in the form of depressed egg numbers, while egg size was conserved, resulting in an estimated 21% reduction in population-level fecundity. These sublethal effects often go undetected and highlight the importance of tracking recovery metrics beyond survival when assessing the impacts of bleaching on coral populations. Bleaching and reproductive output Generally, the capacity for gamete production was maintained in the A. millepora population following bleaching, with only one survivor suffering complete reproductive failure. Early research into the effects of bleaching on reproduction reported mass reproductive cessation, amongst other effects (Baird and Marshall 2002 , Ward et al. 2002 ). Yet since this early research, fecundity responses have varied greatly depending on the region, the species, and the extent and timing of bleaching, and susceptibility has likely changed due to local adaptation. Interestingly, while not reported in Tan et al. 2016 , partial reproductive failure (i.e. some non-reproductive polyps within reproductive branches, or some non-reproductive branches within a reproductive colony) was observed extensively here: we found that A. millepora colonies had significantly fewer eggs in colonies that bleached ‘catastrophically’, although egg size was not significantly reduced (Fig. 4 a, b). These responses may be the result of differential allocation of limited resources to certain polyps or branches (Leinbach et al. 2021 ). However, Tan et al. 2016 preferentially selected polyps containing visible eggs, potentially underestimating partial reproductive failure. While an increase in reproductive output in the years after bleaching has also been reported (Armoza-Zvuloni et al. 2011 ), our study did not indicate a last-ditch effort to reproduce as evidenced by the similarity in overall reproductive output amongst years (Fig. 4 e). Egg size appeared largely unaffected by bleaching, but both the mean number of eggs per polyp and the mean number of eggs per fecund polyp significantly decreased when colonies not bleached (score 6) were compared to those that catastrophically bleached (score 1), equating to a 21% decrease in total egg production. Therefore, colonies appeared to have preferentially conserved egg size over egg number. Egg size is often used in corals as an indicator of health, as smaller eggs are provisioned with less lipids, are less likely to fertilize, and can have shorter larval durations (Levitan 2006 ). The conservation of egg size, but a decrease in egg quantity, is consistent with another study on A. millepora (Jones and Berkelmans 2011 ), and similar findings for another Acropora species have led researchers to conclude that this size-number trade-off may be an Acropora -specific trait (Leinbach et al. 2021 ). The population at large reflected this response; however, variation in egg size amongst sites (Table 1 ) suggests that environmental factors may also influence the degree to which corals are able to provision their eggs. For example, eggs from GKI were nearly 25% larger in volume than eggs from NKI (Fig. 4 b), despite similar levels of bleaching. Interestingly, NKI had some of the highest cumulative heat-stress during the 2020 bleaching event (Page et al. 2023 ), suggesting that this environmental stress may have influenced the provisioning of eggs, irrespective of bleaching score. The concept of coral species as winners and losers in response to heat stress is not new to coral reef ecology (Loya et al. 2001 , van Woesik et al. 2011 ), but the Keppel Islands population of A. millepora appears to act as a ‘winner’ despite exhibiting morphological, biogeographic, and physiological characteristics of a typical ‘loser’: the corymbose morphology of A. millepora is complex in nature, the Keppel Islands lie inshore and are less than 20 km from inputs of terrestrial sediments, nutrients and pollutants, and the species that dominate reefs in this region are considered sensitive, weedy, and fast-growing (Jones and Berkelmans 2014 , Thompson et al. 2022 , Page et al. 2023 ). Despite these factors, A. millepora remains resilient in this region. Previous studies have shown that an increase in heterotrophically-derived nutrition can prevent mortality and aid in rebuilding energy reserves up to a year after bleaching, which is necessary for provisioning eggs (Grottoli et al. 2006 , Hughes and Grottoli 2013 ). Anthony ( 1999 ) demonstrated that A. millepora can have high heterotrophic plasticity; therefore, the highly turbid nature of these reefs may provide greater opportunities for heterotrophic feeding than on lower turbidity mid-shelf and offshore reefs. Bleaching and coral mortality Despite the severe bleaching exhibited by nearly 75% of A. millepora colonies, there was some variability in bleaching response within the population (Fig. 2 ). In general, mortality remained low, and recovery to normal coloration (scores of 5 and 6) occurred for nearly all colonies within six months. Differential bleaching and survival through a marine heat wave can be driven by many factors, including variability in the prevalence of heat-tolerant symbiont communities (Ziegler et al. 2018 , Rowan 2004 , Jones et al. 2008 ). For example, the dominant genera of Symbiodiniaceae hosted can significantly affect coral heat tolerance (Pelosi et al. 2021 ), and symbiont shuffling following bleaching has aided in the speed of coral recovery following past bleaching in the Keppel Islands (Jones et al. 2008 ). Thus, the low mortality observed in the Keppel Islands in 2020 may be due to plasticity in symbiont communities hosted (Jones et al. 2008 , Sweet 2014 , Bay et al. 2016 ). The combination of Cladocopium C3 with Durisdinium -dominated colonies may have also provided some level of heat resilience to A. millepora colonies in this region, as has been previously identified (Berkelmans and van Oppen 2006 , Jones et al. 2008 , Bay et al. 2016 ). Future studies could use amplicon sequencing of multiple markers (Nitschke et al. 2022 ) or map reads from whole genome sequencing studies in samples collected over times to better the role of Symbiodiniaceae in driving bleaching resilience and recovery. Host-specific processes, such as host-environmental memory (Hackerott et al. 2021 ), phenotypic plasticity (Bellantuono et al. 2012 ) and genetic adaptation to bleaching recovery (van Oppen and Blackall 2019 , Marhoefer 2021) may have also contributed to rapid recovery and high survival in this population. An alternative explanation for low mortality following severe bleaching discussed in Page et al. ( 2023 ) is that high turbidity in the region, coupled with large tidal ranges, may have facilitated recovery via three mechanisms: (1) turbidity could have reduced bleaching severity by reducing irradiance stress during periods of anomalously high seawater temperatures (Cacciapaglia and van Woesik 2016 ); (2) increased heterotrophic feeding through the deposition of particulate organic material could have aided recovery (Grottoli 2006); and (3) higher levels of mass transfer with tidal flow may have helped alleviate the build-up of superoxide radicals during bleaching (Loya et al. 2001 ). Shading, feeding and increased flow can all contribute to the resilience of inshore corals, which in this region are known for their exceptional growth rates (Diaz-Pulido et al. 2009 ). Finally, the highly disturbed nature of the system may have already resulted in local adaptation. Reefs in the Keppel Islands are subjected to frequent and varied stresses (Diaz-Pulido et al. 2009 , Thompson et al. 2022 , Page et al. 2023 ). Therefore, it is likely that some level of local adaptation to thermal stress has already occurred, and colonies of A. millepora in the Keppel Islands have been shown to suffer lower background mortality than in other areas of the GBR (Tan et al. 2018 ). The 1998 bleaching event caused nearly 32% whole-colony mortality of fate-tracked A. millepora colonies on the GBR (Baird and Marshall 2002 ). Twenty-two years later, with more heat accumulation than in 1998, mortality was 5-fold lower in the Keppel Islands, suggestive of their higher tolerance to heat stress than central-sector populations of A. millepora historically. Finally, below-average temperatures in the winter months following bleaching also likely offered a reprieve from stress (Randall and van Woesik 2015 ; Page et al. 2023 ), allowing the symbiotic relationship between the coral and their symbionts to recover quickly. Comparison of diver assessed and photo-surveyed bleaching scores There was a strong correlation between the diver-assessed and photo-surveyed scoring methods indicating that the photo-based bleaching assessment captured the scale and severity of bleaching well (Fig. S1). However, occasional discrepancies in diver-assessed scores compared with photo-surveyed scores suggests that the photo-survey method may miss some bleaching, particularly in highly turbid and low-light conditions. For example, one colony scored by divers as ‘severely’ bleached was categorized as ‘negligible’ by the photo-survey method (Fig. S1). Applying uniform lighting near the base of the colonies may significantly improve visibility of interior tissue for ex situ assessments, increasing accuracy. Thus, despite the occasional mismatch, the photo-survey method was fairly reliable and suggests that this approach may prove useful when assessing large datasets or studying large-scale bleaching patterns, particularly with minor improvements in the method e.g. standard camera settings, white balancing using a white/black/grey scale (Hoogenboom et al. 2017 ). The photo-assessment technique can be easily taught and incorporated into citizen science efforts to increase community involvement in reef monitoring and broaden the scale of rapid assessments required during heat waves, while simultaneously increasing community awareness of the current state of reefs in their region. Conclusion Understanding the impacts of bleaching on coral fitness is important for improving predictions of coral population and reef trajectories under climate change. Yet quantifying the impacts on longevity, growth and reproductive output are challenging and are often not captured in acute heat-response studies. Our results suggest that the reproductive output of the Keppel Islands A. millepora population was reduced by 21% in the year following the 2020 mass-bleaching event. Surviving corals are vulnerable to the often under-reported and overlooked sublethal impacts that can persist for a significant period (Johnston et al. 2020), and these effects may be further amplified in populations not adapted to such a highly disturbed and heterotrophic system. Corals that survive the increasing frequency and severity of heat waves predicted under climate change will likely have reduced fitness and reproductive output (Baird and Marshall 2002 , Hagedorn et al. 2016 , Johnston et al. 2020, Leinbach et al. 2021 ). Thus, further studies that assess the impacts of bleaching on coral fitness will improve predictions of coral populations and reef trajectories into the future. Declarations Acknowledgements We acknowledge the Woppaburra People as the traditional Custodians of the Keppel Islands where this research took place. We pay our respects to their Elders past, present, and emerging and acknowledge their continuing spiritual connection to sea Country. All research was conducted with free prior and informed consent (FPIC) from the Woppaburra Traditional Use of Marine Resources Association (TUMRA) committee and was permitted under the Great Barrier Reef Marine Park Authority (GBRMPA) permit G19/43148.1. We thank the crew of the R.V. Cape Ferguson and staff of the Konomie Island Environmental Education Centre for field support. This research was funded by the BHP—AIMS Australian Coral Reef Resilience Initiative. Funding and competing interests This research was funded by the BHP—AIMS Australian Coral Reef Resilience Initiative. The authors declare no competing interests. Data accessibility statement Data are available at the following public archive: https://apps.aims.gov.au/metadata/view/3bbb9779-2179-499d-b27c-77f934e8915d References Anthony KRN (1999) Coral suspension feeding on fine particulate matter. Journal of Experimental Marine Biology and Ecology 232:85–106 Anthony KRN, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, Energetics, and Coral Mortality Risk: Effects of Temperature, Light, and Sediment Regime. Limnology and Oceanography 52:716–726 Armoza-Zvuloni R, Segal R, Kramarsky-Winter E, Loya Y (2011) Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: Oculina patagonica as a model. Marine Ecology Progress Series 426:149–159 Baird A, Marshall P (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237:133–141 Baird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends in Ecology & Evolution 24:16–20 Baria MV, Dela Cruz D, Villanueva R, Guest J (2012) Spawning of three-year-old Acropora millepora corals reared from larvae in Northwestern Philippines. Bulletin of Marine Science 88:6162 Bartoń K (2023) MuMIn: Multi-Model Inference. R package version 1.47.5 Bay LK, Doyle J, Logan M, Berkelmans R (2016) Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. Royal Society Open Science 3:160322 Bellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of the Royal Society B: Biological Sciences 279:1100–1107 Berkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proceedings of the Royal Society B: Biological Sciences 273:2305–2312 Brooks ME, Kristensen K, Benthem KJ van, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) GlmmTMB balances speed and lexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9:378–400 Cacciapaglia C, van Woesik R (2016) Climate-change refugia: shading reef corals by turbidity. Global Change Biology 22:1145–1154 Claar DC, Starko S, Tietjen KL, Epstein HE, Cunning R, Cobb KM, Baker AC, Gates RD, Baum JK (2020) Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves. Nature Communications 11:6097 Cinner, J., Huchery, C., MacNeil, M. et al. Bright spots among the world’s coral reefs. Nature 535, 416–419 (2016). Conlan JA, Bay LK, Jones A, Thompson A, Francis DS (2020) Seasonal variation in the lipid profile of Acropora millepora at Halfway Island, Great Barrier Reef. Coral Reefs 39:1753–1765 Cox EF (2007) Continuation of sexual reproduction in Montipora capitata following bleaching. Coral Reefs 26:721–724 Diaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS One 4:e5239 Eddy TD, Lam VWY, Reygondeau G, Cisneros-Montemayor AM, Greer K, Palomares MLD, Bruno JF, Ota Y, Cheung WWL (2021) Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4:1278–1285 Glynn PW, Colley SB, Maté JL, Baums IB, Feingold JS, Cortés J, Guzmán HM, Afflerbach JC, Brandtneris VW, Ault JS (2012) Reef coral reproduction in the equatorial eastern Pacific: Costa Rica, Panamá, and the Galápagos Islands (Ecuador). VII. Siderastreidae , Psammocora stellata and Psammocora profundacella . Mar Biol 159:1917–1932 Grottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186–1189 Hackerott S, Martell HA, Eirin-Lopez JM (2021) Coral environmental memory: causes, mechanisms, and consequences for future reefs. Trends in Ecology & Evolution 36:1011–1023 Hagedorn M, Carter V, Lager C, Camperio J, Dygert A, Schleiger R, Henley E (2016) Potential bleaching effects on coral reproduction. Reproduction, Fertility and Development 28:1061 Hall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950–963 Harii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral Acropora tenuis . Marine Ecology Progress Series 346:89–96 Harii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Marine Biology 157:1215–1224 Hartig F., (2021). DHARMa: Residual diagnostics for hierarchical (Multi-Level /Mixed) regression models. R package version 0.4.3. https://cran.r-project.org/package=DHARMa Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742 Hoogenboom MO, Frank GE, Chase TJ, Jurriaans S, Álvarez-Noriega M, Peterson K, Critchell K, Berry KLE, Nicolet KJ, Ramsby B, Paley AS (2017) Environmental drivers of variation in bleaching severity of Acropora species during an extreme thermal anomaly. Frontiers in Marine Science 4: van Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L, Williams G, Heron SF, Planes S (2016) Local-scale projections of coral reef futures and implications of the Paris Agreement. Scientific Reports 6:39666 Howells EJ, Bauman AG, Vaughan GO, Hume BCC, Voolstra CR, Burt JA (2020) Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Molecular Ecology 29:899–911 Hughes AD, Grottoli AG (2013) Heterotrophic Compensation: A possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 8:e81172 Hughes TP, Kerry JT, Álvarez-Noriega M, et al. (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377 Hughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018a) Global warming transforms coral reef assemblages. Nature 556:492–496 Hughes TP, Kerry JT, Simpson T (2018b) Large-scale bleaching of corals on the Great Barrier Reef. Ecology 99:501 Johnston EC, Counsell CWW, Sale TL, Burgess SC, Toonen RJ The legacy of stress: Coral bleaching impacts reproduction years later. Functional Ecology 34:2315–2325 Hughes TP, Kerry JT, Baird AH, Connolly SR, Chase TJ, Dietzel A, Hill T, Hoey AS, Hoogenboom MO, Jacobson M, Kerswell A, Madin JS, Mieog A, Paley AS, Pratchett MS, Torda G, Woods RM (2019) Global warming impairs stock–recruitment dynamics of corals. Nature 568:387–390 Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences 275:1359–1365 Jones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant Symbiodinium type-D. Journal of Marine Biology 2011:e185890 Jones AM, Berkelmans R (2014) Flood impacts in Keppel Bay, Southern Great Barrier Reef in the aftermath of cyclonic rainfall. PLOS ONE 9:e84739 Kohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers & Geosciences 32:1259–1269 LaJeunesse T, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt G, Fitt W, Hoegh-Guldberg O (2004) Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress Series 284:147–161 Leinbach SE, Speare KE, Rossin AM, Holstein DM, Strader ME (2021) Energetic and reproductive costs of coral recovery in divergent bleaching responses. Scientific Reports 11:23546 Lenz EA, Bartlett LA, Stathakopoulos A, Kuffner IB (2021) Physiological differences in bleaching response of the coral Porites astreoides along the Florida Keys Reef tract during high-temperature stress. Frontiers in Marine Science 8 Leuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524–531 Levitan D, Boudreau W, Jara J, Knowlton N (2014) Long-term reduced spawning in Orbicella coral species due to temperature stress. Marine Ecology Progress Series 515:1–10 Levitan DR (2006) The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates. Integrative and Comparative Biology 46:298–311 Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecology Letters 4:122–131 Marhoefer SR, Zenger KR, Strugnell JM, Logan M, van Oppen MJH, Kenkel CD, Bay LK (2021) Signatures of Adaptation and Acclimatization to Reef Flat and Slope Habitats in the Coral Pocillopora damicornis . Frontiers in Marine Science 8: Michalek-Wagner K, Willis BL (2001) Impacts of bleaching on the soft coral Lobophytum compactum . I. Fecundity, fertilization and offspring viability. Coral Reefs 19:231–239 Nitschke MR, Rosset SL, Oakley CA, Gardner SG, Camp EF, Suggett DJ, Davy SK (2022) The diversity and ecology of Symbiodiniaceae: A traits-based review. Adv Mar Biol 92:55–127 van Oppen MJH, Lukoschek V, Berkelmans R, Peplow LM, Jones AM (2015) A population genetic assessment of coral recovery on highly disturbed reefs of the Keppel Island archipelago in the southern Great Barrier Reef. PeerJ 3:e1092 van Oppen MJH, Blackall LL (2019) Coral microbiome dynamics, functions and design in a changing world. Nature Reviews Microbiolgy 17:557–567 Page CA, Giuliano C, Bay LK, Randall CJ (2023) High survival following bleaching underscores the resilience of a frequently disturbed region of the Great Barrier Reef. Ecosphere 14:e4280 Pelosi J, Eaton KM, Mychajliw S, terHorst CP, Coffroth MA (2021) Thermally tolerant symbionts may explain Caribbean octocoral resilience to heat stress. Coral Reefs 40:1113–1125 R Core Team (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. Randall C, Szmant A (2009) Elevated Temperature Affects Development, Survivorship, and Settlement of the Elkhorn Coral, Acropora palmata (Lamarck 1816). The Biological bulletin 217:269–82 Randall CJ, Giuliano C, Page CA (2021) No bundles beyond this point: the coral sterile zone. Bulletin of Marine Science 97:75–76 Randall CJ, Negri AP, Quigley KM, Foster T, Ricardo GF, Webster NS, Bay LK, Harrison PL, Babcock RC, Heyward AJ (2020) Sexual production of corals for reef restoration in the Anthropocene. Marine Ecology Progress Series 635:203–232 Randall CJ, van Woesik R (2015) Contemporary white-band disease in Caribbean corals driven by climate change. Nature Climate Change 5:375–379 Rodrigues LJ, Padilla-Gamiño JL (2022) Trophic provisioning and parental trade-offs lead to successful reproductive performance in corals after a bleaching event. Sci Rep 12:18702 Rodríguez-Troncoso AP, Carpizo-Ituarte E, Leyte-Morales GE, Chi-Barragán G, Tapia-Vázquez O (2011) Sexual reproduction of three coral species from the Mexican South Pacific. Marine Biology 158:2673–2683 Rowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742–742 Sakai Y, Hatta M, Furukawa S, Kawata M, Ueno N, Maruyama S (2020) Environmental factors explain spawning day deviation from full moon in the scleractinian coral Acropora. Biology Letters 16:20190760 Sheppard C, Dixon DJ, Gourlay M, Sheppard A, Payet R (2005) Coral mortality increases wave energy reaching shores protected by reef flats: examples from the Seychelles. Estuarine, Coastal and Shelf Science 64:223–234 Shikina S, Chang CF (2016) Sexual Reproduction in Stony Corals and Insight into the Evolution of Oogenesis in Cnidaria. In: Goffredo S., Dubinsky Z. (eds) The Cnidaria, Past, Present and Future: The world of Medusa and her sisters. Springer International Publishing, Cham, pp 249–268 Siebeck UE, Marshall NJ, Klüter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453–460 Sully S, Burkepile DE, Donovan MK, Hodgson G, van Woesik R (2019) A global analysis of coral bleaching over the past two decades. Nat Commun 10:1–5 Sweet MJ (2014) Symbiodinium diversity within Acropora muricata and the surrounding environment. Marine Ecology 35:343–353 Tan C, Pratchett M, Bay L, Graham E, Baird A (2016) Spatial and temporal variation in fecundity among populations of Acropora millepora on the Great Barrier Reef. Marine Ecology Progress Series 561:147–153 Tan CH, Pratchett MS, Bay LK, Graham EM, Baird AH (2018) Biennium horribile: very high mortality in the reef coral Acropora millepora on the Great Barrier Reef in 2009 and 2010. Marine Ecology Progress Series 604:133–142 Thompson A, Davidson J, Logan M, Coleman G (2022) Marine monitoring program: annual report inshore coral reef monitoring 2020-21. Wallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Marine Biology 817:217-233 Ward S, Harrison P, and Hoegh-Guldberg O (2002) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. 9th International Coral Reef Symposium, Bali, Indonesia, 23-27 Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. Woesik R van, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Marine Ecology Progress Series 434:67–76 Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science 314:787–790 Ziegler M, Eguíluz VM, Duarte CM, Voolstra CR (2018) Rare symbionts may contribute to the resilience of coral–algal assemblages. The ISME Journal 12:161–172 Supplementary Figure Figure S1 is not available with this version. Cite Share Download PDF Status: Published Journal Publication published 20 Mar, 2024 Read the published version in Coral Reefs → Version 1 posted 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. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies 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-3346366","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":232370264,"identity":"2391045d-ad35-4c78-86cd-279a44e294bd","order_by":0,"name":"Nico D Briggs","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA30lEQVRIiWNgGAWjYFACHgaGBCDFz8DYQKIWyQaStICAwQFiNZgz8B778OBXrb3x8cOtG38w1MoZHGB+JoFPi2UDX/KMxL7jidvOJLbd5mE4bmxwgM0MrxaDAzzGDIk9xxLMDgC1MDAcS5zZwECcFnvj/odtN3+AtbB/I6wl4UcN4waJxLYbPAw1if0MPARsOcyXzJDYcCBxxo2HQL8YHDDmZ+YptsCr5XjvYcYff+rs+fvTn938UVEnx8bevvEGPi0MzEDM2HYYbilEhDD4Uwdj1eFTNgpGwSgYBSMUAAD0rktzJV/JiQAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0009-0009-9056-8487","institution":"Australian Institute of Marine Science","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Nico","middleName":"D","lastName":"Briggs","suffix":""},{"id":232370265,"identity":"d21def6f-3a6d-40df-bafa-488056d30c4e","order_by":1,"name":"Cathie A Page","email":"","orcid":"https://orcid.org/0000-0003-0779-1629","institution":"Australian Institute of Marine Science","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Cathie","middleName":"A","lastName":"Page","suffix":""},{"id":232370266,"identity":"74a9985c-cad3-4521-bd5d-42dc399d66cd","order_by":2,"name":"Christine Giuliano","email":"","orcid":"https://orcid.org/0000-0002-6945-7151","institution":"Australian Institute of Marine Science","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Christine","middleName":"","lastName":"Giuliano","suffix":""},{"id":232370267,"identity":"ba3ea2bb-d9c6-4cde-beff-db839fd5e62b","order_by":3,"name":"Cinzia Alessi","email":"","orcid":"","institution":"University of New Caledonia","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Cinzia","middleName":"","lastName":"Alessi","suffix":""},{"id":232370268,"identity":"cba354ab-c6c5-4645-95ab-a2915931f122","order_by":4,"name":"Mia Hoogenboom","email":"","orcid":"https://orcid.org/0000-0003-3709-6344","institution":"James Cook University","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Mia","middleName":"","lastName":"Hoogenboom","suffix":""},{"id":232370269,"identity":"2652e6e5-aa58-4d60-9577-caf7adea6a37","order_by":5,"name":"Line K Bay","email":"","orcid":"https://orcid.org/0000-0002-9760-2977","institution":"Australian Institute of Marine Science","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Line","middleName":"K","lastName":"Bay","suffix":""},{"id":232370270,"identity":"bd5b9731-7020-4f69-aeb7-3cabf74597e1","order_by":6,"name":"Carly J Randall","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA4UlEQVRIie3QsQrCMBCA4ZPAdUntGqn4DAEnUdpXiRScKji5OBiXOLoq+Ba+QDFDF+ksOImrg9DRDgZHhWg3wfzzfdwlAC7Xz4bQbnoSslqEIs1qEya+HA6kfy4n04hi63LeHyuIVkw0SmohLPO64bpIKIYjrscKks1akNBGuDkq9BUxRBgiIeGHDD4RcvfV3ByW33RaPQm5fyBotmjzfMp1ihDxXKJ1C9OIfVrk5pPTiXkLE63lQvW2FhIsFTnR6awTePmuTKtBHBCij1cLAfKydSihIW3gvbjeuMvlcv1DDzFDPhE/ZT7gAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0000-0001-8112-3552","institution":"Australian Institute of Marine Science","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Carly","middleName":"J","lastName":"Randall","suffix":""}],"badges":[],"createdAt":"2023-09-11 23:24:56","currentVersionCode":1,"declarations":{"humanSubjects":false,"vertebrateSubjects":false,"conflictsOfInterestStatement":true,"humanSubjectEthicalGuidelines":false,"humanSubjectConsent":false,"humanSubjectClinicalTrial":false,"humanSubjectCaseReport":false,"vertebrateSubjectEthicalGuidelines":false,"coiExplicitlySet":false},"doi":"10.21203/rs.3.rs-3346366/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3346366/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s00338-024-02483-y","type":"published","date":"2024-03-20T11:04:51+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":43145684,"identity":"773eb181-2232-46b8-b072-e9d258c53639","added_by":"auto","created_at":"2023-09-14 17:02:31","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":614945,"visible":true,"origin":"","legend":"\u003cp\u003e(a) Map of the Keppel Islands with four collection sites identified: North Keppel Island (NKI), Pumpkin Island (PI), Great Keppel Island (GKI), and Halfway Island (HI). Background colour represents the mean temperature in February 2020 at the height of the heat wave, at 2.35m depth, as modeled by eReefs (\u003ca href=\"http://www.ereefs.aims.gov.au/\"\u003ewww.ereefs.aims.gov.au\u003c/a\u003e). Figure after Page et al. 2023. (b) Bleaching colour scale, from 1 to 6, based on the CoralWatch Coral Health Chart (Siebeck et al. 2006), and corresponding representative colonies of each score, from in-water surveys in April 2020. Bleaching severity classifications from ‘none’ to ‘catastrophic’ were added alongside nominal scores from the CoralWatch chart, based on our results.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-3346366/v1/9e730b804ac59c6829b51248.png"},{"id":43144980,"identity":"df91aea2-651d-4760-8406-9d79b6e8a3c2","added_by":"auto","created_at":"2023-09-14 16:54:30","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":131459,"visible":true,"origin":"","legend":"\u003cp\u003e(a) Bleaching scores of all tagged colonies (n = 350) and (b) dissected colonies recorded in April 2020 (n = 94), during the height of bleaching at four sites in the Keppel Islands. Colours of the bars represent bleaching scores from most severe (“catastrophic”; score=1) to none (score=6) (Siebeck et al. 2006).\u003cstrong\u003e \u003c/strong\u003e(c) Mean colony diameter against the April 2020 bleaching score with a locally estimated scatterplot smoothing (LOESS) curve and 95% confidence intervals in gray. (d) Logistic model predicting the probability of coral survival as a function of bleaching score, with 95% confidence intervals in gray. Color scales in (c and d) represent bleaching scores from severe (score=1) to none (score=6). Note that points in (d) are jittered along the x-axis for readability.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-3346366/v1/7c9cace9642f1baecf981fa0.png"},{"id":43144981,"identity":"5a6b7d3f-8f1b-404b-bac8-55a291985fe4","added_by":"auto","created_at":"2023-09-14 16:54:30","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":1003638,"visible":true,"origin":"","legend":"\u003cp\u003e\u003cem\u003eAcropora millepora\u003c/em\u003e tissue dissections showing (a) a longitudinal cross section through a branch, and (b) a freshly isolated polyp (left) and a dissected polyp (right) showing spermatozoa (s) and oocytes (o) visible within both primary and secondary mesenteries. White scale bars in (a) and (b) represent 1 mm. Red line segment in (a) represents the length of the sterile zone. Blue line segment in (b) represents the maximum diameter of an oocyte within the mesentery. Photomicrographs: Christine Giuliano.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-3346366/v1/cad1c626f01cc637964a98d7.png"},{"id":43144982,"identity":"818ba87a-bb36-4cf5-adc7-3805f4e9c34f","added_by":"auto","created_at":"2023-09-14 16:54:30","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":75328,"visible":true,"origin":"","legend":"\u003cp\u003eModelled egg size (a, b) and number of eggs per polyp (c, d) by bleaching field score (a, c) and site (b, d) in \u003cem\u003eAcropora millepora\u003c/em\u003e. Asterisk indicates a bleaching score that was significantly different from score 6 in the model (p\u0026lt;0.05). (e) Fecundity in the Keppel Island’s \u003cem\u003eA. millepora\u003c/em\u003e population before (2009, 2010; Tan et al. 2016, 2019 Giuliano, unpublished) and after (2020; present study) bleaching.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-3346366/v1/600a50c0e02d7d0f60797a23.png"},{"id":57205681,"identity":"a122152a-94a1-4f06-9ae2-c35d4ad48dbe","added_by":"auto","created_at":"2024-05-27 11:04:58","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2671292,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3346366/v1/a757c57c-235c-4e3d-a469-62bb8e1f58fb.pdf"}],"financialInterests":"","formattedTitle":"\u003cp\u003eDissecting coral recovery: Bleaching reduces reproductive output in \u003cem\u003eAcropora millepora\u003c/em\u003e\u003c/p\u003e","fulltext":[{"header":"Introduction","content":"\u003cp\u003eCoral reefs support key ecological functions and ecosystem services that are important for humans (Sheppard et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2005\u003c/span\u003e, Worm et al. \u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Cinner et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). However, increasingly frequent climate-change driven disturbance events, including regional scale mass-coral bleaching, have negatively affected coral reefs globally and are challenging the ecosystem\u0026rsquo;s recovery potential (Hughes et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2017\u003c/span\u003e, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2018a\u003c/span\u003e, Sully et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). An estimated 50% of coral cover worldwide has been lost since the 1950s and a downward trajectory is predicted to continue throughout the 21st century (van Hooidonk et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, Eddy et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Consequently, the capacity for coral reefs to support critical ecosystem services is declining (Hughes et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2018b\u003c/span\u003e, Hughes et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2019\u003c/span\u003e, Eddy et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), and the future value of reef systems will depend on their persistence under future climate-change emission scenarios (Hoegh-Guldberg et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2007\u003c/span\u003e, Chen et al. 2015).\u003c/p\u003e \u003cp\u003eRecovery and persistence of reefs after disturbances is driven by the growth of surviving colonies (van Oppen et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) and by larval recruitment from sexual reproduction (Glynn et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). Larval supply comes from both mass-spawning events (i.e., the synchronous release of gametes by spawning corals at particular times of the year), and from brooding corals, which experience internal fertilization and then release fully developed larvae (Sakai et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). In both cases, reproduction is energetically costly, requiring a build-up of energy reserves prior to spawning (Leuzinger et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2003\u003c/span\u003e, Anthony et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). Coral eggs are comprised of proteins, carbohydrates, and lipids, which aid in embryo floatation and provide an energy source for the developing larvae (Harii et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2007\u003c/span\u003e, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). The accumulation of lipids and other macromolecules is directly impacted by the breakdown of the coral host-symbiont relationship and the resulting decline in nutrition from the symbiont to the coral host (Conlan et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2020\u003c/span\u003e, Rodrigues and Padilla-Gami\u0026ntilde;o \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Energy use by corals is also altered during bleaching and can lead to physiological trade-offs, including the differential partitioning of energy between gamete production and colony maintenance (Rodrigues and Padilla-Gami\u0026ntilde;o \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Due to the annual reproductive cycle in many coral species, oocyte maturation and/or spawning often coincides with summer heat-stress (Randall et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), Shikina and Chang \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), increasing the potential for bleaching to impact reproductive output. Therefore, understanding how bleaching events influence the production of coral gametes, and subsequent supply of larvae to degraded reefs, can inform our understanding of the recovery capacity of coral populations and communities.\u003c/p\u003e \u003cp\u003eTo date, three primary effects of heat-stress on coral reproduction have been documented and include, in decreasing order of severity: (i) complete failure of gametogenesis; (ii) a decrease in fecundity; and (iii) a decline in gamete viability. Firstly, complete failure to produce gametes is the most well-documented sublethal impact of bleaching on coral reproduction (Ward et al. \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2002\u003c/span\u003e, Levitan et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2014\u003c/span\u003e) and has been recorded during heat-stress conditions even when colonies showed no visible signs of bleaching (Rodriguez-Troncoso et al. 2011). Secondly, a decline in metrics of reproductive output such as egg size and fecundity has been observed in response to bleaching (Michalek-Wagner and Willis \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2001\u003c/span\u003e, Baird and Marshall \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2002\u003c/span\u003e, Ward et al. \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2002\u003c/span\u003e, Cox \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). For example, Jones and Berkelmans (\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2011\u003c/span\u003e) found that bleached \u003cem\u003eAcropora millepora\u003c/em\u003e colonies produced smaller and 50% fewer eggs, and that the proportion of colonies within the population that were reproductive had declined. Thirdly, some studies have demonstrated an effect of bleaching on gamete and larval viability. For example, Hagedorn et al. (\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2016\u003c/span\u003e) documented a decline in sperm motility and fertilization rates following bleaching, while an increase in developmental abnormalities and a decline in larval survival in response to direct heat stress has been observed (Randall and Szmant \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2009\u003c/span\u003e, Lenz et al. \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). While most studies examine the immediate impacts of heat stress or bleaching on reproduction, how long these effects persist following heat stress and colony recovery remains unclear. Furthermore, variability in the persistence of these sublethal effects has been noted across species, geographic regions and environmental regimes. Therefore, continuing to investigate the potential long-term sub-lethal impacts of bleaching on species and reefs is critically important for predicting coral responses to future climate warming.\u003c/p\u003e \u003cp\u003eSevere and widespread bleaching occurred within Woppaburra sea Country (the Keppel Islands, southern inshore Great Barrier Reef (GBR)) in March - April 2020. Although mortality was low (Page et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), it was unknown whether the surviving corals suffered any impacts to reproduction in the spawning season following bleaching. Furthermore, individual bleaching responses were highly variable, and the relationship between bleaching severity and post-bleaching reproductive output is not well documented (Leinbach et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). To address these knowledge gaps, we tagged \u003cem\u003eAcropora millepora\u003c/em\u003e colonies during bleaching and tracked their fates over six months. Colonies that spanned the full spectrum of bleaching phenotypes, from none to catastrophic, were then sampled, decalcified, and dissected to address the following research questions: (i) what is the relationship between bleaching severity and fecundity? (ii) how does post-bleaching fecundity compare with historical baselines? (iii) are bleaching severity, colony size, and coral mortality related?\u003c/p\u003e"},{"header":"Methods","content":"\u003ch2\u003eSite selection, sample collection and decalcification\u003c/h2\u003e\n\u003cp\u003eThis study was conducted on fringing reefs in the Keppel Islands of the southern inshore GBR. Four sites were selected across the Island group: Great Keppel Island (GKI, 23.1030\u0026deg; S 150.5740\u0026deg; E), North Keppel Island (NKI, 23.0738\u0026deg; S, 150.8987\u0026deg; E), Halfway Island (HI, 23.1984\u0026deg; S, 150.9718\u0026deg; E), and Pumpkin Island (PI, 23.0927\u0026deg; S, 150.9011\u0026deg; E) (Fig. \u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e) and were at 1 to 5 m depth below lowest astronomical tide (LAT). \u003cem\u003eAcropora millepora\u003c/em\u003e is a corymbose species common across Woppaburra sea Country where it has been extensively studied (Jones and Berkelmans \u003cspan class=\"CitationRef\"\u003e2011\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003eBetween 18 and 21 April 2020, at the height of the heatwave induced bleaching, 350 adult \u003cem\u003eA. millepora\u003c/em\u003e colonies (~\u0026thinsp;10\u0026ndash;75 cm maximum diameter, average\u0026thinsp;=\u0026thinsp;30 cm) were haphazardly tagged across sites, to capture a wide range of bleaching phenotypes within the populations. Colonies were tagged at each of NKI (n\u0026thinsp;=\u0026thinsp;100), PI (n\u0026thinsp;=\u0026thinsp;101), HI (n\u0026thinsp;=\u0026thinsp;99), and GKI (n\u0026thinsp;=\u0026thinsp;50). During tagging, colonies were assigned an \u003cem\u003ein situ\u003c/em\u003e ordinal bleaching score that ranged from 1 to 6, based on the CoralWatch Coral Health Chart (Siebeck et al. \u003cspan class=\"CitationRef\"\u003e2006\u003c/span\u003e) and were photographed (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e\n\u003cp\u003eBetween 7 and 17 October 2020, approximately 1 month prior to the predicted coral spawning (realized on 9 Nov 2020 for colonies from the population (C. Randall personal observation)) and approximately 6 months following the height of bleaching, 311 tagged colonies were re-surveyed and the following data were recorded: (i) mortality status (dead or alive), (ii) percentage of live tissue remaining in intervals of 10% (i.e. 10\u0026ndash;100% live tissue), (iii) maximum diameter (cm), (iv) maximum perpendicular diameter (cm), and (v) bleaching score (1\u0026ndash;6), as described above. Colonies that were not sampled at the second time point (n\u0026thinsp;=\u0026thinsp;39) were excluded from analysis. Estimated surface area of live tissue \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\left(SA\\right)\\)\u003c/span\u003e\u003c/span\u003e was calculated for each colony from the maximum diameter (\u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(a\\)\u003c/span\u003e\u003c/span\u003e) and the maximum perpendicular diameter (\u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(b\\)\u003c/span\u003e\u003c/span\u003e), both of which were recorded across a horizontal plane by a diver, using Eq. 1: \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(SA = \\pi \\left(\\frac{1}{2}a\\right)\\left(\\frac{1}{2}b\\right)\\)\u003c/span\u003e\u003c/span\u003e.Mean colony diameter was also calculated from \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(a\\)\u003c/span\u003e\u003c/span\u003e and \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(b\\)\u003c/span\u003e\u003c/span\u003e.\u003c/p\u003e\n\u003cp\u003eDuring resurvey, three replicate branches were sampled from the central area of each colony to avoid the sterile zone found at the outer margins of \u003cem\u003eAcropora\u003c/em\u003e colonies (Wallace \u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e, Randall et al. \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e). Branches were collected using a small chisel or knife and were placed in pre-labeled sample bags with seawater. Immediately post dive, coral samples were transferred to a solution of 10% formaldehyde in 1 \u0026micro;m filtered seawater (FSW) (hereafter \u0026lsquo;formalin\u0026rsquo;). Samples were then transferred into 3% hydrochloric acid (HCl) in FSW solution for decalcification, and additional 3% HCl was added over a few days to replenish the weak acid until complete decalcification of the branches had occurred (decalcification durations varied from 3 to 10 days). Decalcified tissue samples were rinsed in FSW and stored in fresh formalin until dissection.\u003c/p\u003e\n\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e\n \u003ch2\u003eSample dissection\u003c/h2\u003e\n \u003cp\u003eDecalcified samples from a total of 94 colonies were dissected to assess fecundity. Colonies were systematically chosen for dissection to ensure an even representation across the range of bleaching phenotypes and, where possible, sites (Fig. \u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003eb).\u003c/p\u003e\n \u003cp\u003eBranches were dissected under a Lecia M60 Stereomicroscope at 20x \u0026minus;\u0026thinsp;40x magnification. Measurements were taken at 25x magnification from live image (5mp digital C-mount camera) within ToupView software. Maximum branch length was measured with digital calipers, and then a longitudinal section was cut through the middle of the branch, which was suspended in FSW in a wax dish, using a scalpel (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003ea). The length of the sterile zone\u0026mdash; the tip of \u003cem\u003eAcropora\u003c/em\u003e branches where the newest growth lacks gonads (Wallace \u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e)\u0026mdash;was clearly visible from the longitudinal section and measured from the apical polyp tip to the nearest visibly fecund polyp (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003ea). Ten polyps were haphazardly selected from near the base of the branch, with the branch interior facing downward, in order to minimize bias in selecting polyps that had visible eggs; polyps were then removed with forceps and dissected as per Wallace \u003cspan class=\"CitationRef\"\u003e1985\u003c/span\u003e (Fig. \u003cspan class=\"InternalRef\"\u003e3\u003c/span\u003eb). Very small polyps were avoided, although smaller than average polyps were sometimes selected as a result of the haphazard process and, in most instances, were observed to be reproductively mature. The number of polyps (out of 10) that had successfully produced oocytes was recorded. Then, the number of oocytes within each polyp was counted, and for each of the first three polyps containing eggs, the maximum diameter \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\left(d\\right)\\)\u003c/span\u003e\u003c/span\u003e was recorded for each egg observed. Egg volume (\u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(V\\)\u003c/span\u003e\u003c/span\u003e) was then estimated using Eq. 2: \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(V=\\frac{4}{3}\\pi {\\left(\\frac{d}{2}\\right)}^{3}\\)\u003c/span\u003e\u003c/span\u003e, assuming a sphere.\u003c/p\u003e\n \u003c/div\u003e\n\u003cdiv id=\"Sec4\" class=\"Section2\"\u003e\n \u003ch2\u003eStatistical Analysis\u003c/h2\u003e\n \u003cp\u003eAll statistical analyses were completed in R (R Core Team, \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e). Generalized linear mixed effect models (GLMM) utilizing a template model builder (Brooks et al. \u003cspan class=\"CitationRef\"\u003e2017\u003c/span\u003e) were used to model reproductive output. Models were created to test for the additive effects of bleaching score, site, and mean colony diameter on three reproductive metrics: (1) egg size, (2) number of eggs per polyp, and (3) number of eggs per fecund polyp. Replicate branch within colony, and colony within site were treated as nested random effects in the model of egg size. In the models of egg numbers, only colony within site was treated as a nested random effect due to a lack of convergence in the full model. All response variables (egg size, number of eggs per polyp, and number of eggs per fecund polyp) were modelled with a Gaussian distribution. A null model was formulated using only random effects and model selection was undertaken by comparing models with each combination of predictors against the null model, using second-order Akaike Information Criterion (AICc) in the MuMIn package (Bartoń 2013). Analysis of Variance (ANOVA) was used to statistically compare models and validate model selection. Based on this model selection method, site and mean diameter were not included in the final models of number of eggs per polyp and number of eggs per fecund polyp. Model assumptions were assessed and validated using DHARMa residual analysis (Hartig \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e) and results were visualized using \u0026lsquo;ggplot2\u0026rsquo; (Wickham \u003cspan class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e\n \u003cp\u003eColony size does not appear to determine reproductive output of each polyp in \u003cem\u003eA. millepora\u003c/em\u003e once coral maturation is reached at approximately 15 cm in diameter (Hall and Hughes \u003cspan class=\"CitationRef\"\u003e1996\u003c/span\u003e, Baria et al. \u003cspan class=\"CitationRef\"\u003e2012\u003c/span\u003e). Therefore, two colonies from NKI that were less than 15 cm diameter were excluded from the analysis. Samples from HI were also removed from the site-specific models due to a comparatively small sample size (HI n\u0026thinsp;=\u0026thinsp;4, PI n\u0026thinsp;=\u0026thinsp;29, NKI n\u0026thinsp;=\u0026thinsp;34, GKI n\u0026thinsp;=\u0026thinsp;27). Therefore, a total of 88 colonies were included in the models testing site-level variation, and 92 colonies were included in fecundity models.\u003c/p\u003e\n \u003cp\u003eTo investigate the relationship between bleaching score and colony survival, a logistic regression with a binomial distribution and a logit link function was modelled using \u0026lsquo;glm\u0026rsquo; from the \u0026lsquo;stats\u0026rsquo; package and diagnostics were checked as described above (R Core Team, \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec5\" class=\"Section2\"\u003e\n \u003ch2\u003eHistorical Data\u003c/h2\u003e\n \u003cp\u003eThree years of historical \u003cem\u003eA. millepora\u003c/em\u003e fecundity data from the Keppel Islands were used to establish a baseline of reproductive output prior to recent bleaching. Firstly, Tan et al. (\u003cspan class=\"CitationRef\"\u003e2016\u003c/span\u003e) measured the number of eggs per polyp from haphazardly selected \u003cem\u003eA. millepora\u003c/em\u003e colonies in a manner comparable to this study, in 2009 and 2010, prior to the 2016 and 2017 bleaching events. Secondly, following the sampling methods described above, a single branch from 49 haphazardly sampled colonies from 10 sites across the Keppel Islands in October 2019 (6 months before bleaching) were dissected, 12\u0026ndash;19 days prior to 2019 spawning. To determine whether reproductive output in 2020 differed from these baselines, we modelled the number of eggs per polyp against year using a general linear model with a Gaussian distribution, as described above.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec6\" class=\"Section2\"\u003e\n \u003ch2\u003eEstimate of population level reduction in fecundity\u003c/h2\u003e\n \u003cp\u003eBased on the results of this study, a population level fecundity reduction was estimated from the bleaching data that were collected from all 310 colonies surveyed during bleaching in April 2020. Firstly, a hypothetical population-level fecundity potential was calculated, in the absence of bleaching. To do this, we first assumed a sterile zone of length 7.3 mm around the colony perimeter as per the mean sterile zone measured from all replicates. We then re-calculated the maximum fecund diameter (\u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(a\\)\u003c/span\u003e\u003c/span\u003e) and maximum fecund perpendicular diameter \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\left(b\\right)\\)\u003c/span\u003e\u003c/span\u003e for each colony by subtracting 14.6 mm (7.3 mm on each side) from each metric and used those values to calculate a \u0026lsquo;fecund SA\u0026rsquo; in cm\u003csup\u003e2\u003c/sup\u003e for each colony using Eq.\u0026nbsp;1. The total number of fecund polyps per colony was then estimated by multiplying the fecund SA of planar area measured by diameter (in cm\u003csup\u003e2\u003c/sup\u003e) by the average density of polyps in \u003cem\u003eAcropora millepora\u003c/em\u003e (87 polyps cm\u003csup\u003e\u0026minus;\u0026thinsp;2\u003c/sup\u003e; Hall and Hughes \u003cspan class=\"CitationRef\"\u003e1996\u003c/span\u003e). From this, the modelled number of eggs per polyp, assuming no bleaching (score\u0026thinsp;=\u0026thinsp;6; 7.47 eggs per polyp), was multiplied by the number of reproductive polyps per colony, to create a baseline assumption of a colony\u0026rsquo;s potential reproductive output, if healthy. Then, to account for bleaching and partial mortality, the number of fecund polyps for each colony was reduced by the % reduction in egg number estimated for that colony\u0026rsquo;s bleaching score and then reduced by the % partial mortality observed, to estimate a realized reproductive output following bleaching. For colonies that suffered complete mortality, realized reproductive output was zero. Finally, the percentage reduction between the hypothetical reproductive output and the estimated realized reproductive output for all colonies combined was calculated, providing an estimate of the impact of the 2020 bleaching event on population-level fecundity. We note that this method assumes a planar SA and thus likely underestimates the colony-level reproductive potential, although the estimated percentage reduction should scale proportionally.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec7\" class=\"Section2\"\u003e\n \u003ch2\u003eComparison of diver assessed and photo-surveyed bleaching scores\u003c/h2\u003e\n \u003cp\u003eTo assess whether field images of colonies could be used to accurately identify bleaching severity, bleaching scores were estimated from images taken in April 2020 using Coral Point Count with Excel Extensions (CPCe), from 10 randomly placed points overlaid on each colony, excluding those points that fell on the growing tips of the colonies, which are naturally paler than the surrounding colony (Kohler et al. 2006). The relationship between \u003cem\u003ein situ\u003c/em\u003e diver assessed and \u003cem\u003eex situ\u003c/em\u003e photo-surveyed bleaching scores was tested using a Pearson\u0026rsquo;s correlation coefficient with the function cor.test in base R (R Core Team \u003cspan class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e\n\u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eOf the colonies phenotyped during the height of bleaching (April 2020), 61% had a severe bleaching response (category\u0026thinsp;=\u0026thinsp;2, n\u0026thinsp;=\u0026thinsp;214) while 15% had a catastrophic response (category\u0026thinsp;=\u0026thinsp;1, n\u0026thinsp;=\u0026thinsp;53), together accounting for 76% of all colonies scored (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003ea). Only 4.5% of colonies did not visually bleach (category\u0026thinsp;=\u0026thinsp;6, n\u0026thinsp;=\u0026thinsp;16). Whole-colony mortality was highest at PI (17%, n\u0026thinsp;=\u0026thinsp;16) while no whole-colony mortality was observed at NKI (SI Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e, Page et al. \u003cspan class=\"CitationRef\"\u003e2023\u003c/span\u003e). The likelihood of survival significantly increased as a function of bleaching score (GLM: z\u0026thinsp;=\u0026thinsp;3.437, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001) (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003ed); only \u0026lsquo;catastrophically\u0026rsquo; and \u0026lsquo;severely\u0026rsquo; bleached colonies (scores of 1 and 2, respectively) suffered whole-colony mortality (2.9% in score 1 (n\u0026thinsp;=\u0026thinsp;9) and 3.5% in score 2 (n\u0026thinsp;=\u0026thinsp;11), which equated to an overall mortality of 6.5% (n\u0026thinsp;=\u0026thinsp;20). Partial mortality ranged from 10\u0026ndash;90%, but occurred rarely (incidence of 2%), and only in severely bleached colonies (score of 2, n\u0026thinsp;=\u0026thinsp;6). As colony size increased, the bleaching response became more severe (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e2\u003c/span\u003ec). Nearly all colonies had recovered by October, with an average score of 5 (\u0026lsquo;negligible\u0026rsquo; bleaching) at all sites at that time, with only two colonies retaining a \u0026lsquo;mild\u0026rsquo; level of bleaching (score 3, n\u0026thinsp;=\u0026thinsp;2).\u003c/p\u003e\n\u003ch3\u003eEgg Number\u003c/h3\u003e\n\u003cp\u003ePolyp fecundity (number of eggs per polyp and number of eggs per fecund polyp) significantly differed by bleaching score, but not by site (Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e, Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003ec, d). Egg output per polyp decreased by approximately 21% from the least bleached (7.5 eggs per polyp) to the most bleached (5.9 eggs per polyp) colonies (SE\u0026thinsp;=\u0026thinsp;0.77, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;=\u0026thinsp;\u0026lt;\u0026thinsp;0.05), with similar results in the egg output per fecund polyp model (SE\u0026thinsp;=\u0026thinsp;0.63, \u003cem\u003ep\u0026thinsp;=\u0026thinsp;\u0026lt;\u003c/em\u003e\u0026thinsp;0.05) (Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). While egg output differed in the overall models between scores of 1 and 6, pairwise post-hoc Tukey tests showed no significant pairwise differences in either model.\u003c/p\u003e\n\u003cdiv id=\"Sec10\" class=\"Section2\"\u003e\n \u003ch2\u003eEgg Size\u003c/h2\u003e\n \u003cp\u003eBleaching score was not a significant predictor of egg size, although site and colony diameter were (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003ea, b). Eggs from GKI colonies were 0.05 mm larger than eggs from NKI colonies (SE\u0026thinsp;=\u0026thinsp;0.01, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.0001) and 0.04 mm larger than eggs from PI colonies (SE\u0026thinsp;=\u0026thinsp;0.01, \u003cem\u003ep\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.01) (Table\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e). These size estimates equate to an approximate 10% difference in egg diameter, and a consequent 25% difference in egg volume between GKI and NKI.\u003c/p\u003e\n \u003cdiv class=\"gridtable\"\u003e\n \u003ctable id=\"Tab1\" border=\"1\"\u003e\n \u003ccaption language=\"En\"\u003e\n \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e\n \u003cdiv class=\"CaptionContent\"\u003e\n \u003cp\u003eEstimated marginal mean (emmean) egg size, number of eggs per polyp, and number of eggs per fecund polyp modelled against bleaching field score and site as fixed effects. Site abbreviations are as in Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e1\u003c/span\u003e.\u003c/p\u003e\n \u003c/div\u003e\n \u003c/caption\u003e\n \u003cthead\u003e\n \u003ctr\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003eFecundity Metric\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003eBest Model\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003eBleaching score/ Site\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003eemmean\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003eSE\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003edf\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\"\u003e\n \u003cp\u003e\u003cem\u003elower.CL\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003cth align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e\u003cem\u003eupper.CL\u003c/em\u003e\u003c/p\u003e\n \u003c/th\u003e\n \u003c/tr\u003e\n \u003c/thead\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" rowspan=\"9\"\u003e\n \u003cp\u003e\u003cstrong\u003eMean Egg Size\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" rowspan=\"6\"\u003e\n \u003cp\u003eFecundity\u0026thinsp;~\u0026thinsp;Field Score\u0026thinsp;+\u0026thinsp;Site\u0026thinsp;+\u0026thinsp;Mean Diameter + (1|Sample/Rep)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.53\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.008\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.516\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.549\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.011\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.515\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.557\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.026\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.489\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.591\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.56\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.017\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.527\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.594\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.010\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.523\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.563\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.55\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.013\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.528\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.580\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" rowspan=\"3\"\u003e\n \u003cp\u003eFecundity\u0026thinsp;~\u0026thinsp;Field Score\u0026thinsp;+\u0026thinsp;Site\u0026thinsp;+\u0026thinsp;Mean Diameter + (1|Sample/Rep)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eGKI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.57\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.009\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.557\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.591\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eNKI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.52\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.010\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.503\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.541\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ePI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.009\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e770\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.519\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e0.555\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" rowspan=\"9\"\u003e\n \u003cp\u003e\u003cstrong\u003eMean # of Eggs Per Polyp\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" rowspan=\"6\"\u003e\n \u003cp\u003eFecundity\u0026thinsp;~\u0026thinsp;Field Score + (1|Sample)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.9\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.402\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e252\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.109\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e6.694\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.04\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.497\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e252\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.065\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.023\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e1.251\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e252\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e4.125\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e9.052\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.29\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.819\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e252\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e4.677\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.903\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e7.08\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.511\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e252\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.070\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e8.085\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e7.47\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.653\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e252\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.180\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e8.753\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" rowspan=\"3\"\u003e\n \u003cp\u003eFecundity\u0026thinsp;~\u0026thinsp;Field Score\u0026thinsp;+\u0026thinsp;Site + (1|Sample)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eGKI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.434\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e250\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.743\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.451\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eNKI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.65\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.504\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e250\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.661\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.646\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ePI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.46\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.450\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e250\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.572\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.341\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" rowspan=\"9\"\u003e\n \u003cp\u003e\u003cstrong\u003eMean # of Eggs Per Fecund Polyp\u003c/strong\u003e\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" rowspan=\"6\"\u003e\n \u003cp\u003eFecundity\u0026thinsp;~\u0026thinsp;Field Score + (1|Sample)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e1\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.22\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.330\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e248\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.575\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e6.873\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e2\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.73\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.419\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e248\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.900\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.551\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e3\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e7.11\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e1.025\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e248\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.089\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e9.126\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e4\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.57\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.671\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e248\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e5.245\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.887\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e5\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e7.16\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.419\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e248\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.336\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e7.987\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e6\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e7.68\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.535\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e248\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.630\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"2\"\u003e\n \u003cp\u003e8.738\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\" rowspan=\"3\"\u003e\n \u003cp\u003eFecundity\u0026thinsp;~\u0026thinsp;Field Score\u0026thinsp;+\u0026thinsp;Site + (1|Sample)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eGKI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.86\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.355\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e246\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.162\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e7.562\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"1\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003eNKI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.91\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.413\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e246\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.095\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e7.722\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"1\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003ePI\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.97\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e0.373\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e246\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"char\"\u003e\n \u003cp\u003e6.239\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\"\u003e\n \u003cp\u003e7.707\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd align=\"left\" colspan=\"1\"\u003e\u0026nbsp;\u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n \u003c/table\u003e\n \u003c/div\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec11\" class=\"Section2\"\u003e\n \u003ch2\u003ePopulation-level fecundity\u003c/h2\u003e\n \u003cp\u003eBased on the estimate of fecundity for each bleaching score, combined with whole-colony and partial mortality, we estimated a 21% reduction in total oocyte output of the population six months after the 2020 bleaching event.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec12\" class=\"Section2\"\u003e\n \u003ch2\u003eCoral fecundity past and present\u003c/h2\u003e\n \u003cp\u003eMean number of eggs per fecund polyp in 2020 did not differ from pre-bleaching baselines (Fig.\u0026nbsp;\u003cspan class=\"InternalRef\"\u003e4\u003c/span\u003ee). Samples from 2019 and unbleached samples in 2020 (scores of 5 and 6) had a higher mean polyp fecundity than compared to the historic baseline, but bleached colonies in 2020 (scores of 1 and 2) had a similar or lower polyp fecundity than historic baselines.\u003c/p\u003e\n\u003c/div\u003e\n\u003cdiv id=\"Sec13\" class=\"Section2\"\u003e\n \u003ch2\u003eComparison of diver assessed and photo-surveyed bleaching scores\u003c/h2\u003e\n \u003cp\u003eDiver assessed and photo surveyed (CPCe) bleaching scores were tightly and positively correlated (t\u0026thinsp;=\u0026thinsp;29.99, df\u0026thinsp;=\u0026thinsp;348, p\u0026thinsp;\u0026lt;\u0026thinsp;0.001, r\u0026thinsp;=\u0026thinsp;0.85) (Fig. S1). The greatest variance in CPCe score was found for colonies with field scores of 2 and 3, while the least variance was seen for colonies at either end of the scale (scores 1 and 6). However, some colonies scored as \u0026lsquo;severe\u0026rsquo; (score\u0026thinsp;=\u0026thinsp;2) by divers \u003cem\u003ein situ\u003c/em\u003e were scored as not bleached by the CPCe method, indicating the potential for some underestimation of bleaching from images (Fig. S1).\u003c/p\u003e\n\u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eSevere bleaching occurred throughout Woppaburra sea Country (the Keppel Islands) during the 2020 marine heatwave, but mortality of \u003cem\u003eAcropora millepora\u003c/em\u003e was low (~\u0026thinsp;6.5% this study; Page et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Despite recovery by the time of coral spawning six months later, we found that heavily bleached colonies experienced a significant reduction in reproductive output in the form of depressed egg numbers, while egg size was conserved, resulting in an estimated 21% reduction in population-level fecundity. These sublethal effects often go undetected and highlight the importance of tracking recovery metrics beyond survival when assessing the impacts of bleaching on coral populations.\u003c/p\u003e \u003cdiv id=\"Sec15\" class=\"Section2\"\u003e \u003ch2\u003eBleaching and reproductive output\u003c/h2\u003e \u003cp\u003eGenerally, the capacity for gamete production was maintained in the \u003cem\u003eA. millepora\u003c/em\u003e population following bleaching, with only one survivor suffering complete reproductive failure. Early research into the effects of bleaching on reproduction reported mass reproductive cessation, amongst other effects (Baird and Marshall \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2002\u003c/span\u003e, Ward et al. \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Yet since this early research, fecundity responses have varied greatly depending on the region, the species, and the extent and timing of bleaching, and susceptibility has likely changed due to local adaptation. Interestingly, while not reported in Tan et al. \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2016\u003c/span\u003e, partial reproductive failure (i.e. some non-reproductive polyps within reproductive branches, or some non-reproductive branches within a reproductive colony) was observed extensively here: we found that \u003cem\u003eA. millepora\u003c/em\u003e colonies had significantly fewer eggs in colonies that bleached \u0026lsquo;catastrophically\u0026rsquo;, although egg size was not significantly reduced (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ea, b). These responses may be the result of differential allocation of limited resources to certain polyps or branches (Leinbach et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). However, Tan et al. \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2016\u003c/span\u003e preferentially selected polyps containing visible eggs, potentially underestimating partial reproductive failure. While an increase in reproductive output in the years after bleaching has also been reported (Armoza-Zvuloni et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), our study did not indicate a last-ditch effort to reproduce as evidenced by the similarity in overall reproductive output amongst years (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ee).\u003c/p\u003e \u003cp\u003eEgg size appeared largely unaffected by bleaching, but both the mean number of eggs per polyp and the mean number of eggs per fecund polyp significantly decreased when colonies not bleached (score 6) were compared to those that catastrophically bleached (score 1), equating to a 21% decrease in total egg production. Therefore, colonies appeared to have preferentially conserved egg size over egg number. Egg size is often used in corals as an indicator of health, as smaller eggs are provisioned with less lipids, are less likely to fertilize, and can have shorter larval durations (Levitan \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). The conservation of egg size, but a decrease in egg quantity, is consistent with another study on \u003cem\u003eA. millepora\u003c/em\u003e (Jones and Berkelmans \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), and similar findings for another \u003cem\u003eAcropora\u003c/em\u003e species have led researchers to conclude that this size-number trade-off may be an \u003cem\u003eAcropora\u003c/em\u003e-specific trait (Leinbach et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The population at large reflected this response; however, variation in egg size amongst sites (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e) suggests that environmental factors may also influence the degree to which corals are able to provision their eggs. For example, eggs from GKI were nearly 25% larger in volume than eggs from NKI (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eb), despite similar levels of bleaching. Interestingly, NKI had some of the highest cumulative heat-stress during the 2020 bleaching event (Page et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), suggesting that this environmental stress may have influenced the provisioning of eggs, irrespective of bleaching score.\u003c/p\u003e \u003cp\u003eThe concept of coral species as winners and losers in response to heat stress is not new to coral reef ecology (Loya et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2001\u003c/span\u003e, van Woesik et al. \u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), but the Keppel Islands population of \u003cem\u003eA. millepora\u003c/em\u003e appears to act as a \u0026lsquo;winner\u0026rsquo; despite exhibiting morphological, biogeographic, and physiological characteristics of a typical \u0026lsquo;loser\u0026rsquo;: the corymbose morphology of \u003cem\u003eA. millepora\u003c/em\u003e is complex in nature, the Keppel Islands lie inshore and are less than 20 km from inputs of terrestrial sediments, nutrients and pollutants, and the species that dominate reefs in this region are considered sensitive, weedy, and fast-growing (Jones and Berkelmans \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2014\u003c/span\u003e, Thompson et al. \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Page et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Despite these factors, \u003cem\u003eA. millepora\u003c/em\u003e remains resilient in this region. Previous studies have shown that an increase in heterotrophically-derived nutrition can prevent mortality and aid in rebuilding energy reserves up to a year after bleaching, which is necessary for provisioning eggs (Grottoli et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Hughes and Grottoli \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Anthony (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1999\u003c/span\u003e) demonstrated that \u003cem\u003eA. millepora\u003c/em\u003e can have high heterotrophic plasticity; therefore, the highly turbid nature of these reefs may provide greater opportunities for heterotrophic feeding than on lower turbidity mid-shelf and offshore reefs.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec16\" class=\"Section2\"\u003e \u003ch2\u003eBleaching and coral mortality\u003c/h2\u003e \u003cp\u003eDespite the severe bleaching exhibited by nearly 75% of \u003cem\u003eA. millepora\u003c/em\u003e colonies, there was some variability in bleaching response within the population (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). In general, mortality remained low, and recovery to normal coloration (scores of 5 and 6) occurred for nearly all colonies within six months. Differential bleaching and survival through a marine heat wave can be driven by many factors, including variability in the prevalence of heat-tolerant symbiont communities (Ziegler et al. \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e2018\u003c/span\u003e, Rowan \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2004\u003c/span\u003e, Jones et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). For example, the dominant genera of Symbiodiniaceae hosted can significantly affect coral heat tolerance (Pelosi et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), and symbiont shuffling following bleaching has aided in the speed of coral recovery following past bleaching in the Keppel Islands (Jones et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). Thus, the low mortality observed in the Keppel Islands in 2020 may be due to plasticity in symbiont communities hosted (Jones et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2008\u003c/span\u003e, Sweet \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2014\u003c/span\u003e, Bay et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). The combination of \u003cem\u003eCladocopium\u003c/em\u003e C3 with \u003cem\u003eDurisdinium\u003c/em\u003e-dominated colonies may have also provided some level of heat resilience to \u003cem\u003eA. millepora\u003c/em\u003e colonies in this region, as has been previously identified (Berkelmans and van Oppen \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2006\u003c/span\u003e, Jones et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2008\u003c/span\u003e, Bay et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Future studies could use amplicon sequencing of multiple markers (Nitschke et al. \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2022\u003c/span\u003e) or map reads from whole genome sequencing studies in samples collected over times to better the role of Symbiodiniaceae in driving bleaching resilience and recovery. Host-specific processes, such as host-environmental memory (Hackerott et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), phenotypic plasticity (Bellantuono et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2012\u003c/span\u003e) and genetic adaptation to bleaching recovery (van Oppen and Blackall \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2019\u003c/span\u003e, Marhoefer 2021) may have also contributed to rapid recovery and high survival in this population.\u003c/p\u003e \u003cp\u003eAn alternative explanation for low mortality following severe bleaching discussed in Page et al. (\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e) is that high turbidity in the region, coupled with large tidal ranges, may have facilitated recovery via three mechanisms: (1) turbidity could have reduced bleaching severity by reducing irradiance stress during periods of anomalously high seawater temperatures (Cacciapaglia and van Woesik \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2016\u003c/span\u003e); (2) increased heterotrophic feeding through the deposition of particulate organic material could have aided recovery (Grottoli 2006); and (3) higher levels of mass transfer with tidal flow may have helped alleviate the build-up of superoxide radicals during bleaching (Loya et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2001\u003c/span\u003e). Shading, feeding and increased flow can all contribute to the resilience of inshore corals, which in this region are known for their exceptional growth rates (Diaz-Pulido et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). Finally, the highly disturbed nature of the system may have already resulted in local adaptation. Reefs in the Keppel Islands are subjected to frequent and varied stresses (Diaz-Pulido et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2009\u003c/span\u003e, Thompson et al. \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2022\u003c/span\u003e, Page et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Therefore, it is likely that some level of local adaptation to thermal stress has already occurred, and colonies of \u003cem\u003eA. millepora\u003c/em\u003e in the Keppel Islands have been shown to suffer lower background mortality than in other areas of the GBR (Tan et al. \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). The 1998 bleaching event caused nearly 32% whole-colony mortality of fate-tracked \u003cem\u003eA. millepora\u003c/em\u003e colonies on the GBR (Baird and Marshall \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Twenty-two years later, with more heat accumulation than in 1998, mortality was 5-fold lower in the Keppel Islands, suggestive of their higher tolerance to heat stress than central-sector populations of \u003cem\u003eA. millepora\u003c/em\u003e historically. Finally, below-average temperatures in the winter months following bleaching also likely offered a reprieve from stress (Randall and van Woesik \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Page et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2023\u003c/span\u003e), allowing the symbiotic relationship between the coral and their symbionts to recover quickly.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec17\" class=\"Section2\"\u003e \u003ch2\u003eComparison of diver assessed and photo-surveyed bleaching scores\u003c/h2\u003e \u003cp\u003eThere was a strong correlation between the diver-assessed and photo-surveyed scoring methods indicating that the photo-based bleaching assessment captured the scale and severity of bleaching well (Fig. S1). However, occasional discrepancies in diver-assessed scores compared with photo-surveyed scores suggests that the photo-survey method may miss some bleaching, particularly in highly turbid and low-light conditions. For example, one colony scored by divers as \u0026lsquo;severely\u0026rsquo; bleached was categorized as \u0026lsquo;negligible\u0026rsquo; by the photo-survey method (Fig. S1). Applying uniform lighting near the base of the colonies may significantly improve visibility of interior tissue for \u003cem\u003eex situ\u003c/em\u003e assessments, increasing accuracy. Thus, despite the occasional mismatch, the photo-survey method was fairly reliable and suggests that this approach may prove useful when assessing large datasets or studying large-scale bleaching patterns, particularly with minor improvements in the method e.g. standard camera settings, white balancing using a white/black/grey scale (Hoogenboom et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). The photo-assessment technique can be easily taught and incorporated into citizen science efforts to increase community involvement in reef monitoring and broaden the scale of rapid assessments required during heat waves, while simultaneously increasing community awareness of the current state of reefs in their region.\u003c/p\u003e \u003c/div\u003e"},{"header":"Conclusion","content":"\u003cp\u003eUnderstanding the impacts of bleaching on coral fitness is important for improving predictions of coral population and reef trajectories under climate change. Yet quantifying the impacts on longevity, growth and reproductive output are challenging and are often not captured in acute heat-response studies. Our results suggest that the reproductive output of the Keppel Islands \u003cem\u003eA. millepora\u003c/em\u003e population was reduced by 21% in the year following the 2020 mass-bleaching event. Surviving corals are vulnerable to the often under-reported and overlooked sublethal impacts that can persist for a significant period (Johnston et al. 2020), and these effects may be further amplified in populations not adapted to such a highly disturbed and heterotrophic system. Corals that survive the increasing frequency and severity of heat waves predicted under climate change will likely have reduced fitness and reproductive output (Baird and Marshall \u003cspan class=\"CitationRef\"\u003e2002\u003c/span\u003e, Hagedorn et al. \u003cspan class=\"CitationRef\"\u003e2016\u003c/span\u003e, Johnston et al. 2020, Leinbach et al. \u003cspan class=\"CitationRef\"\u003e2021\u003c/span\u003e). Thus, further studies that assess the impacts of bleaching on coral fitness will improve predictions of coral populations and reef trajectories into the future.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eAcknowledgements\u003c/h2\u003e \u003cp\u003eWe acknowledge the Woppaburra People as the traditional Custodians of the Keppel Islands where this research took place. We pay our respects to their Elders past, present, and emerging and acknowledge their continuing spiritual connection to sea Country. All research was conducted with free prior and informed consent (FPIC) from the Woppaburra Traditional Use of Marine Resources Association (TUMRA) committee and was permitted under the Great Barrier Reef Marine Park Authority (GBRMPA) permit G19/43148.1. We thank the crew of the R.V. Cape Ferguson and staff of the Konomie Island Environmental Education Centre for field support. This research was funded by the BHP\u0026mdash;AIMS Australian Coral Reef Resilience Initiative.\u003c/p\u003e\n\u003ch2\u003eFunding and competing interests\u003c/h2\u003e\n\u003cp\u003eThis research was funded by the BHP\u0026mdash;AIMS Australian Coral Reef Resilience Initiative. The authors declare no competing interests.\u003c/p\u003e\n\u003ch2\u003eData accessibility statement\u003c/h2\u003e\n\u003cp\u003eData are available at the following public archive: https://apps.aims.gov.au/metadata/view/3bbb9779-2179-499d-b27c-77f934e8915d\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAnthony KRN (1999) Coral suspension feeding on fine particulate matter. Journal of Experimental Marine Biology and Ecology 232:85\u0026ndash;106 \u003c/li\u003e\n\u003cli\u003eAnthony KRN, Connolly SR, Hoegh-Guldberg O (2007) Bleaching, Energetics, and Coral Mortality Risk: Effects of Temperature, Light, and Sediment Regime. Limnology and Oceanography 52:716\u0026ndash;726 \u003c/li\u003e\n\u003cli\u003eArmoza-Zvuloni R, Segal R, Kramarsky-Winter E, Loya Y (2011) Repeated bleaching events may result in high tolerance and notable gametogenesis in stony corals: \u003cem\u003eOculina\u003c/em\u003e \u003cem\u003epatagonica\u003c/em\u003e as a model. Marine Ecology Progress Series 426:149\u0026ndash;159 \u003c/li\u003e\n\u003cli\u003eBaird A, Marshall P (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 237:133\u0026ndash;141 \u003c/li\u003e\n\u003cli\u003eBaird AH, Bhagooli R, Ralph PJ, Takahashi S (2009) Coral bleaching: the role of the host. Trends in Ecology \u0026amp; Evolution 24:16\u0026ndash;20\u003c/li\u003e\n\u003cli\u003eBaria MV, Dela Cruz D, Villanueva R, Guest J (2012) Spawning of three-year-old \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003emillepora\u003c/em\u003e corals reared from larvae in Northwestern Philippines. Bulletin of Marine Science 88:6162\u003c/li\u003e\n\u003cli\u003eBartoń K (2023) MuMIn: Multi-Model Inference. R package version 1.47.5\u003c/li\u003e\n\u003cli\u003eBay LK, Doyle J, Logan M, Berkelmans R (2016) Recovery from bleaching is mediated by threshold densities of background thermo-tolerant symbiont types in a reef-building coral. Royal Society Open Science 3:160322 \u003c/li\u003e\n\u003cli\u003eBellantuono AJ, Hoegh-Guldberg O, Rodriguez-Lanetty M (2012) Resistance to thermal stress in corals without changes in symbiont composition. Proceedings of the Royal Society B: Biological Sciences 279:1100\u0026ndash;1107 \u003cbr\u003e \u003c/li\u003e\n\u003cli\u003eBerkelmans R, van Oppen MJH (2006) The role of zooxanthellae in the thermal tolerance of corals: a \u0026lsquo;nugget of hope\u0026rsquo; for coral reefs in an era of climate change. Proceedings of the Royal Society B: Biological Sciences 273:2305\u0026ndash;2312 \u003c/li\u003e\n\u003cli\u003eBrooks ME, Kristensen K, Benthem KJ van, Magnusson A, Berg CW, Nielsen A, Skaug HJ, M\u0026auml;chler M, Bolker BM (2017) GlmmTMB balances speed and lexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal 9:378\u0026ndash;400 \u003c/li\u003e\n\u003cli\u003eCacciapaglia C, van Woesik R (2016) Climate-change refugia: shading reef corals by turbidity. Global Change Biology 22:1145\u0026ndash;1154 \u003c/li\u003e\n\u003cli\u003eClaar DC, Starko S, Tietjen KL, Epstein HE, Cunning R, Cobb KM, Baker AC, Gates RD, Baum JK (2020) Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves. Nature Communications 11:6097 \u003c/li\u003e\n\u003cli\u003eCinner, J., Huchery, C., MacNeil, M. et al. Bright spots among the world\u0026rsquo;s coral reefs. Nature 535, 416\u0026ndash;419 (2016). \u003c/li\u003e\n\u003cli\u003eConlan JA, Bay LK, Jones A, Thompson A, Francis DS (2020) Seasonal variation in the lipid profile of \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003emillepora\u003c/em\u003e at Halfway Island, Great Barrier Reef. Coral Reefs 39:1753\u0026ndash;1765 \u003c/li\u003e\n\u003cli\u003eCox EF (2007) Continuation of sexual reproduction in \u003cem\u003eMontipora\u003c/em\u003e \u003cem\u003ecapitata\u003c/em\u003e following bleaching. Coral Reefs 26:721\u0026ndash;724\u003c/li\u003e\n\u003cli\u003eDiaz-Pulido G, McCook LJ, Dove S, Berkelmans R, Roff G, Kline DI, Weeks S, Evans RD, Williamson DH, Hoegh-Guldberg O (2009) Doom and boom on a resilient reef: climate change, algal overgrowth and coral recovery. PLoS One 4:e5239\u003c/li\u003e\n\u003cli\u003eEddy TD, Lam VWY, Reygondeau G, Cisneros-Montemayor AM, Greer K, Palomares MLD, Bruno JF, Ota Y, Cheung WWL (2021) Global decline in capacity of coral reefs to provide ecosystem services. One Earth 4:1278\u0026ndash;1285\u003c/li\u003e\n\u003cli\u003eGlynn PW, Colley SB, Mat\u0026eacute; JL, Baums IB, Feingold JS, Cort\u0026eacute;s J, Guzm\u0026aacute;n HM, Afflerbach JC, Brandtneris VW, Ault JS (2012) Reef coral reproduction in the equatorial eastern Pacific: Costa Rica, Panam\u0026aacute;, and the Gal\u0026aacute;pagos Islands (Ecuador). VII. \u003cem\u003eSiderastreidae\u003c/em\u003e, \u003cem\u003ePsammocora\u003c/em\u003e \u003cem\u003estellata\u003c/em\u003e and \u003cem\u003ePsammocora\u003c/em\u003e \u003cem\u003eprofundacella\u003c/em\u003e. Mar Biol 159:1917\u0026ndash;1932 \u003c/li\u003e\n\u003cli\u003eGrottoli AG, Rodrigues LJ, Palardy JE (2006) Heterotrophic plasticity and resilience in bleached corals. Nature 440:1186\u0026ndash;1189 \u003c/li\u003e\n\u003cli\u003eHackerott S, Martell HA, Eirin-Lopez JM (2021) Coral environmental memory: causes, mechanisms, and consequences for future reefs. Trends in Ecology \u0026amp; Evolution 36:1011\u0026ndash;1023\u003c/li\u003e\n\u003cli\u003eHagedorn M, Carter V, Lager C, Camperio J, Dygert A, Schleiger R, Henley E (2016) Potential bleaching effects on coral reproduction. Reproduction, Fertility and Development 28:1061\u003c/li\u003e\n\u003cli\u003eHall VR, Hughes TP (1996) Reproductive strategies of modular organisms: comparative studies of reef-building corals. Ecology 77:950\u0026ndash;963\u003c/li\u003e\n\u003cli\u003eHarii S, Nadaoka K, Yamamoto M, Iwao K (2007) Temporal changes in settlement, lipid content and lipid composition of larvae of the spawning hermatypic coral \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003etenuis\u003c/em\u003e. Marine Ecology Progress Series 346:89\u0026ndash;96\u003c/li\u003e\n\u003cli\u003eHarii S, Yamamoto M, Hoegh-Guldberg O (2010) The relative contribution of dinoflagellate photosynthesis and stored lipids to the survivorship of symbiotic larvae of the reef-building corals. Marine Biology 157:1215\u0026ndash;1224\u003c/li\u003e\n\u003cli\u003eHartig F., (2021). DHARMa: Residual diagnostics for hierarchical (Multi-Level /Mixed) regression models. R package version 0.4.3. https://cran.r-project.org/package=DHARMa \u003c/li\u003e\n\u003cli\u003eHoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737\u0026ndash;1742\u003c/li\u003e\n\u003cli\u003eHoogenboom MO, Frank GE, Chase TJ, Jurriaans S, \u0026Aacute;lvarez-Noriega M, Peterson K, Critchell K, Berry KLE, Nicolet KJ, Ramsby B, Paley AS (2017) Environmental drivers of variation in bleaching severity of \u003cem\u003eAcropora\u003c/em\u003e species during an extreme thermal anomaly. Frontiers in Marine Science 4:\u003c/li\u003e\n\u003cli\u003evan Hooidonk R, Maynard J, Tamelander J, Gove J, Ahmadia G, Raymundo L, Williams G, Heron SF, Planes S (2016) Local-scale projections of coral reef futures and implications of the Paris Agreement. Scientific Reports 6:39666\u003c/li\u003e\n\u003cli\u003eHowells EJ, Bauman AG, Vaughan GO, Hume BCC, Voolstra CR, Burt JA (2020) Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Molecular Ecology 29:899\u0026ndash;911\u003c/li\u003e\n\u003cli\u003eHughes AD, Grottoli AG (2013) Heterotrophic Compensation: A possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 8:e81172\u003c/li\u003e\n\u003cli\u003eHughes TP, Kerry JT, \u0026Aacute;lvarez-Noriega M, et al. (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373\u0026ndash;377\u003c/li\u003e\n\u003cli\u003eHughes TP, Kerry JT, Baird AH, Connolly SR, Dietzel A, Eakin CM, Heron SF, Hoey AS, Hoogenboom MO, Liu G, McWilliam MJ, Pears RJ, Pratchett MS, Skirving WJ, Stella JS, Torda G (2018a) Global warming transforms coral reef assemblages. Nature 556:492\u0026ndash;496\u003c/li\u003e\n\u003cli\u003eHughes TP, Kerry JT, Simpson T (2018b) Large-scale bleaching of corals on the Great Barrier Reef. Ecology 99:501 \u003c/li\u003e\n\u003cli\u003eJohnston EC, Counsell CWW, Sale TL, Burgess SC, Toonen RJ The legacy of stress: Coral bleaching impacts reproduction years later. Functional Ecology 34:2315\u0026ndash;2325\u003c/li\u003e\n\u003cli\u003eHughes TP, Kerry JT, Baird AH, Connolly SR, Chase TJ, Dietzel A, Hill T, Hoey AS, Hoogenboom MO, Jacobson M, Kerswell A, Madin JS, Mieog A, Paley AS, Pratchett MS, Torda G, Woods RM (2019) Global warming impairs stock\u0026ndash;recruitment dynamics of corals. Nature 568:387\u0026ndash;390\u003c/li\u003e\n\u003cli\u003eJones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W (2008) A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences 275:1359\u0026ndash;1365\u003c/li\u003e\n\u003cli\u003eJones AM, Berkelmans R (2011) Tradeoffs to thermal acclimation: energetics and reproduction of a reef coral with heat tolerant \u003cem\u003eSymbiodinium\u003c/em\u003e type-D. Journal of Marine Biology 2011:e185890\u003c/li\u003e\n\u003cli\u003eJones AM, Berkelmans R (2014) Flood impacts in Keppel Bay, Southern Great Barrier Reef in the aftermath of cyclonic rainfall. PLOS ONE 9:e84739\u003c/li\u003e\n\u003cli\u003eKohler KE, Gill SM (2006) Coral Point Count with Excel extensions (CPCe): A Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers \u0026amp; Geosciences 32:1259\u0026ndash;1269\u003c/li\u003e\n\u003cli\u003eLaJeunesse T, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt G, Fitt W, Hoegh-Guldberg O (2004) Closely related \u003cem\u003eSymbiodinium\u003c/em\u003e spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress Series 284:147\u0026ndash;161\u003c/li\u003e\n\u003cli\u003eLeinbach SE, Speare KE, Rossin AM, Holstein DM, Strader ME (2021) Energetic and reproductive costs of coral recovery in divergent bleaching responses. Scientific Reports 11:23546\u003c/li\u003e\n\u003cli\u003eLenz EA, Bartlett LA, Stathakopoulos A, Kuffner IB (2021) Physiological differences in bleaching response of the coral \u003cem\u003ePorites\u003c/em\u003e \u003cem\u003eastreoides\u003c/em\u003e along the Florida Keys Reef tract during high-temperature stress. Frontiers in Marine Science 8\u003c/li\u003e\n\u003cli\u003eLeuzinger S, Anthony KRN, Willis BL (2003) Reproductive energy investment in corals: scaling with module size. Oecologia 136:524\u0026ndash;531\u003c/li\u003e\n\u003cli\u003eLevitan D, Boudreau W, Jara J, Knowlton N (2014) Long-term reduced spawning in \u003cem\u003eOrbicella\u003c/em\u003e coral species due to temperature stress. Marine Ecology Progress Series 515:1\u0026ndash;10\u003c/li\u003e\n\u003cli\u003eLevitan DR (2006) The relationship between egg size and fertilization success in broadcast-spawning marine invertebrates. Integrative and Comparative Biology 46:298\u0026ndash;311\u003c/li\u003e\n\u003cli\u003eLoya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecology Letters 4:122\u0026ndash;131\u003c/li\u003e\n\u003cli\u003eMarhoefer SR, Zenger KR, Strugnell JM, Logan M, van Oppen MJH, Kenkel CD, Bay LK (2021) Signatures of Adaptation and Acclimatization to Reef Flat and Slope Habitats in the Coral \u003cem\u003ePocillopora\u003c/em\u003e \u003cem\u003edamicornis\u003c/em\u003e. Frontiers in Marine Science 8: \u003c/li\u003e\n\u003cli\u003eMichalek-Wagner K, Willis BL (2001) Impacts of bleaching on the soft coral \u003cem\u003eLobophytum\u003c/em\u003e \u003cem\u003ecompactum\u003c/em\u003e. I. Fecundity, fertilization and offspring viability. Coral Reefs 19:231\u0026ndash;239\u003c/li\u003e\n\u003cli\u003eNitschke MR, Rosset SL, Oakley CA, Gardner SG, Camp EF, Suggett DJ, Davy SK (2022) The diversity and ecology of Symbiodiniaceae: A traits-based review. Adv Mar Biol 92:55\u0026ndash;127 \u003c/li\u003e\n\u003cli\u003evan Oppen MJH, Lukoschek V, Berkelmans R, Peplow LM, Jones AM (2015) A population genetic assessment of coral recovery on highly disturbed reefs of the Keppel Island archipelago in the southern Great Barrier Reef. PeerJ 3:e1092\u003c/li\u003e\n\u003cli\u003evan Oppen MJH, Blackall LL (2019) Coral microbiome dynamics, functions and design in a changing world. Nature Reviews Microbiolgy 17:557\u0026ndash;567 \u003c/li\u003e\n\u003cli\u003ePage CA, Giuliano C, Bay LK, Randall CJ (2023) High survival following bleaching underscores the resilience of a frequently disturbed region of the Great Barrier Reef. Ecosphere 14:e4280\u003c/li\u003e\n\u003cli\u003ePelosi J, Eaton KM, Mychajliw S, terHorst CP, Coffroth MA (2021) Thermally tolerant symbionts may explain Caribbean octocoral resilience to heat stress. Coral Reefs 40:1113\u0026ndash;1125\u003c/li\u003e\n\u003cli\u003eR Core Team (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/. \u003c/li\u003e\n\u003cli\u003eRandall C, Szmant A (2009) Elevated Temperature Affects Development, Survivorship, and Settlement of the Elkhorn Coral, \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003epalmata\u003c/em\u003e (Lamarck 1816). The Biological bulletin 217:269\u0026ndash;82\u003c/li\u003e\n\u003cli\u003eRandall CJ, Giuliano C, Page CA (2021) No bundles beyond this point: the coral sterile zone. Bulletin of Marine Science 97:75\u0026ndash;76\u003c/li\u003e\n\u003cli\u003eRandall CJ, Negri AP, Quigley KM, Foster T, Ricardo GF, Webster NS, Bay LK, Harrison PL, Babcock RC, Heyward AJ (2020) Sexual production of corals for reef restoration in the Anthropocene. Marine Ecology Progress Series 635:203\u0026ndash;232\u003c/li\u003e\n\u003cli\u003eRandall CJ, van Woesik R (2015) Contemporary white-band disease in Caribbean corals driven by climate change. Nature Climate Change 5:375\u0026ndash;379\u003c/li\u003e\n\u003cli\u003eRodrigues LJ, Padilla-Gami\u0026ntilde;o JL (2022) Trophic provisioning and parental trade-offs lead to successful reproductive performance in corals after a bleaching event. Sci Rep 12:18702\u003c/li\u003e\n\u003cli\u003eRodr\u0026iacute;guez-Troncoso AP, Carpizo-Ituarte E, Leyte-Morales GE, Chi-Barrag\u0026aacute;n G, Tapia-V\u0026aacute;zquez O (2011) Sexual reproduction of three coral species from the Mexican South Pacific. Marine Biology 158:2673\u0026ndash;2683\u003c/li\u003e\n\u003cli\u003eRowan R (2004) Thermal adaptation in reef coral symbionts. Nature 430:742\u0026ndash;742\u003c/li\u003e\n\u003cli\u003eSakai Y, Hatta M, Furukawa S, Kawata M, Ueno N, Maruyama S (2020) Environmental factors explain spawning day deviation from full moon in the scleractinian coral Acropora. Biology Letters 16:20190760\u003c/li\u003e\n\u003cli\u003eSheppard C, Dixon DJ, Gourlay M, Sheppard A, Payet R (2005) Coral mortality increases wave energy reaching shores protected by reef flats: examples from the Seychelles. Estuarine, Coastal and Shelf Science 64:223\u0026ndash;234\u003c/li\u003e\n\u003cli\u003eShikina S, Chang CF (2016) Sexual Reproduction in Stony Corals and Insight into the Evolution of Oogenesis in Cnidaria. In: Goffredo S., Dubinsky Z. (eds) The Cnidaria, Past, Present and Future: The world of Medusa and her sisters. Springer International Publishing, Cham, pp 249\u0026ndash;268\u003c/li\u003e\n\u003cli\u003eSiebeck UE, Marshall NJ, Kl\u0026uuml;ter A, Hoegh-Guldberg O (2006) Monitoring coral bleaching using a colour reference card. Coral Reefs 25:453\u0026ndash;460\u003c/li\u003e\n\u003cli\u003eSully S, Burkepile DE, Donovan MK, Hodgson G, van Woesik R (2019) A global analysis of coral bleaching over the past two decades. Nat Commun 10:1\u0026ndash;5\u003c/li\u003e\n\u003cli\u003eSweet MJ (2014) \u003cem\u003eSymbiodinium\u003c/em\u003e diversity within \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003emuricata\u003c/em\u003e and the surrounding environment. Marine Ecology 35:343\u0026ndash;353\u003c/li\u003e\n\u003cli\u003eTan C, Pratchett M, Bay L, Graham E, Baird A (2016) Spatial and temporal variation in fecundity among populations of \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003emillepora\u003c/em\u003e on the Great Barrier Reef. Marine Ecology Progress Series 561:147\u0026ndash;153\u003c/li\u003e\n\u003cli\u003eTan CH, Pratchett MS, Bay LK, Graham EM, Baird AH (2018) Biennium horribile: very high mortality in the reef coral \u003cem\u003eAcropora\u003c/em\u003e \u003cem\u003emillepora\u003c/em\u003e on the Great Barrier Reef in 2009 and 2010. Marine Ecology Progress Series 604:133\u0026ndash;142\u003c/li\u003e\n\u003cli\u003eThompson A, Davidson J, Logan M, Coleman G (2022) Marine monitoring program: annual report inshore coral reef monitoring 2020-21.\u003c/li\u003e\n\u003cli\u003eWallace CC (1985) Reproduction, recruitment and fragmentation in nine sympatric species of the coral genus Acropora. Marine Biology 817:217-233\u003c/li\u003e\n\u003cli\u003eWard S, Harrison P, and Hoegh-Guldberg O (2002) Coral bleaching reduces reproduction of scleractinian corals and increases susceptibility to future stress. 9th International Coral Reef Symposium, Bali, Indonesia, 23-27\u003c/li\u003e\n\u003cli\u003eWickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York.\u003c/li\u003e\n\u003cli\u003eWoesik R van, Sakai K, Ganase A, Loya Y (2011) Revisiting the winners and the losers a decade after coral bleaching. Marine Ecology Progress Series 434:67\u0026ndash;76 \u003c/li\u003e\n\u003cli\u003eWorm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, Jackson JBC, Lotze HK, Micheli F, Palumbi SR, Sala E, Selkoe KA, Stachowicz JJ, Watson R (2006) Impacts of Biodiversity Loss on Ocean Ecosystem Services. Science 314:787\u0026ndash;790\u003c/li\u003e\n\u003cli\u003eZiegler M, Egu\u0026iacute;luz VM, Duarte CM, Voolstra CR (2018) Rare symbionts may contribute to the resilience of coral\u0026ndash;algal assemblages. The ISME Journal 12:161\u0026ndash;172\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Supplementary Figure","content":"\u003cp\u003eFigure S1 is not available with this version.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"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":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Fecundity, egg size, bleaching severity, sublethal effects, climate change, ocean warming","lastPublishedDoi":"10.21203/rs.3.rs-3346366/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3346366/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eIncreasingly frequent and severe bleaching events driven by climate change are decreasing coral populations worldwide. Recovery of these populations relies on reproduction by the survivors of such events including local and upstream larval sources. Yet, corals that survive bleaching may be impaired by sublethal effects that suppress reproduction, reducing larval input to reefs, and consequently impeding recovery. We investigated the impact of the 2020 mass-bleaching event on \u003cem\u003eAcropora millepora\u003c/em\u003e reproduction on inshore, turbid reefs in Woppaburra sea Country (the Keppel Islands), to improve our understanding of the effects of bleaching on coral populations. \u003cem\u003eA. millepora\u003c/em\u003e experienced high bleaching incidence but low mortality across the island group during this event and thus constituted an ideal population to investigate potential sublethal effects on reproductive output. Six months after the heat wave, and just prior to spawning, we collected, decalcified, and dissected samples from 94 tagged \u003cem\u003eA. millepora\u003c/em\u003e colonies with a known 2020 bleaching response, to investigate the relationships between stress severity and reproduction. Despite having regained their pigmentation, we detected a significant reduction in fecundity in colonies that had bleached severely. Considering the impact of the bleaching event on the coral population sampled (i.e. mortality, bleaching severity and colony size), coupled with reductions in fecundity, we estimated a total decrease in population-level reproductive output of 21%. These results suggest that reduced reproductive output may impact recovery of coral populations following bleaching and should be considered alongside traditional estimates from coral mortality.\u003c/p\u003e","manuscriptTitle":"Dissecting coral recovery: Bleaching reduces reproductive output in Acropora millepora","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-09-14 16:54:25","doi":"10.21203/rs.3.rs-3346366/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"3fc99f9e-c303-4816-95bb-cc6f9a3f4ed1","owner":[],"postedDate":"September 14th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":24549419,"name":"Marine and Freshwater Ecology"}],"tags":[],"updatedAt":"2024-05-27T11:04:51+00:00","versionOfRecord":{"articleIdentity":"rs-3346366","link":"https://doi.org/10.1007/s00338-024-02483-y","journal":{"identity":"coral-reefs","isVorOnly":false,"title":"Coral Reefs"},"publishedOn":"2024-03-20 11:04:51","publishedOnDateReadable":"March 20th, 2024"},"versionCreatedAt":"2023-09-14 16:54:25","video":"","vorDoi":"10.1007/s00338-024-02483-y","vorDoiUrl":"https://doi.org/10.1007/s00338-024-02483-y","workflowStages":[]},"version":"v1","identity":"rs-3346366","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3346366","identity":"rs-3346366","version":["v1"]},"buildId":"wLkW0s4AflPzk-lpfg-fK","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}