Multi-Factor Coral Disease Risk: A new product for early warning and management.

Ecological forecasts are becoming increasingly valuable tools for conservation and management. However, there are few examples of near-real-time forecasting systems that account for the wide range of ecological complexities. We developed a new coral disease ecological forecasting system that explores a suite of ecological relationships and their uncertainty and investigates how forecast skill changes with shorter lead times. The Multi-Factor Coral Disease Risk product introduced here uses a combination of ecological and marine environmental conditions to predict the risk of white syndromes and growth anomalies across reefs in the central and western Pacific and along the east coast of Australia and is available through the US National Oceanic and Atmospheric Administration Coral Reef Watch program. This product produces weekly forecasts for a moving window of 6 months at a resolution of ~5 km based on quantile regression forests. The forecasts show superior skill at predicting disease risk on withheld survey data from 2012 to 2020 compared with predecessor forecast systems, with the biggest improvements shown for predicting disease risk at mid- to high-disease levels. Most of the prediction uncertainty arises from model uncertainty, so prediction accuracy and precision do not improve substantially with shorter lead times. This result arises because many predictor variables cannot be accurately forecasted, which is a common challenge across ecosystems. Weekly forecasts and scenarios can be explored through an online decision support tool and data explorer, co-developed with end-user groups to improve use and understanding of ecological forecasts. The models provide near-real-time disease risk assessments and allow users to refine predictions and assess intervention scenarios. This work advances the field of ecological forecasting with real-world complexities and, in doing so, better supports near-term decision making for coral reef ecosystem managers and stakeholders. Secondarily, we identify clear needs and provide recommendations to further enhance our ability to forecast coral disease risk.

Microplastics absent from reef fish in the Marshall Islands: Multistage screening methods reduced false positives.

Island communities, like the Republic of the Marshall Islands (RMI), depend on marine resources for food and economics, so plastic ingestion by those resources is a concern. The gastrointestinal tracts of nine species of reef fish across five trophic groups (97 fish) were examined for plastics >1 mm. Over 2100 putative plastic particles from 72 fish were identified under light microscopy. Only 115 of these from 47 fish passed a plastic screening method using Fourier-transform infrared microspectroscopy (µFTIR) in reflectance mode. All of these were identified as natural materials in a final confirmatory analysis, attenuated total reflectance FTIR. The high false-positive rate of visual and µFTIR methods highlight the importance of using multiple polymer identification methods. Limited studies on ingested plastic in reef fish present challenging comparisons because of different methods used. No plastic >1 mm were found in the RMI reef fish, reassuring human consumers.

Evidence for managing herbivores for reef resilience.

Herbivore management is an important tool for resilience-based approaches to coral reef conservation, and evidence-based science is needed to enact successful management. We synthesized data from multiple monitoring programs in Hawai'i to measure herbivore biomass and benthic condition over a 10-year period preceding any major coral bleaching. We analysed data from 20 242 transects alongside data on 27 biophysical and human drivers and found herbivore biomass was highly variable throughout Hawai'i, with high values in remote locations and the lowest values near population centres. Both human and biophysical drivers explained variation in herbivore biomass, and among the human drivers both fishing and land-based pollution had negative effects on biomass. We also found evidence that herbivore functional group biomass is strongly linked to benthic condition, and that benthic condition is sensitive to changes in herbivore biomass associated with fishing. We show that when herbivore biomass is below 80% of potential biomass, benthic condition is predicted to decline. We also show that a range of management actions, including area-specific fisheries regulations and gear restrictions, can increase parrotfish biomass. Together, these results provide lines of evidence to support managing herbivores as an effective strategy for maintaining or bolstering reef resilience in a changing climate.

Spatial extent of dysbiosis in the branching coral Pocillopora damicornis during an acute disease outbreak.

Globally, coral reefs face increasing disease prevalence and large-scale outbreak events. These outbreaks offer insights into microbial and functional patterns of coral disease, including early indicators of disease that may be present in visually-healthy tissues. Outbreak events also allow investigation of how reef-building corals, typically colonial organisms, respond to disease. We studied Pocillopora damicornis during an acute tissue loss disease outbreak on Guam to determine whether dysbiosis was present in visually-healthy tissues ahead of advancing disease lesions. These data reveal that coral fragments with visual evidence of disease are expectedly dysbiotic with high microbial and metabolomic variability. However, visually-healthy tissues from the same colonies lacked dysbiosis, suggesting disease containment near the affected area. These results challenge the idea of using broad dysbiosis as a pre-visual disease indicator and prompt reevaluation of disease assessment in colonial organisms such as reef-building corals.

A systematic review and meta-analysis of the direct effects of nutrients on corals.

Chronic exposure of coral reefs to elevated nutrient conditions can modify the performance of the coral holobiont and shift the competitive interactions of reef organisms. Many studies have now quantified the links between nutrients and coral performance, but few have translated these studies to directly address coastal water quality standards. To address this management need, we conducted a systematic review of peer-reviewed studies, public reports, and gray literature that examined the impacts of dissolved inorganic nitrogen (DIN: nitrate, nitrite, and ammonium) and dissolved inorganic phosphorus (DIP: phosphate) on scleractinian corals. The systematic review resulted in 47 studies with comparable data on coral holobiont responses to nutrients: symbiont density, chlorophyll a (chl-a) concentration, photosynthesis, photosynthetic efficiency, growth, calcification, adult survival, juvenile survival, and fertilization. Mixed-effects meta-regression meta-analyses were used to determine the magnitude of the positive or negative effects of DIN and DIP on coral responses. Zooxanthellae density (DIN & DIP), chl-a concentration (DIN), photosynthetic rate (DIN), and growth (DIP) all exhibited positive responses to nutrient addition; maximum quantum yield (DIP), growth (DIN), larval survival (DIN), and fertilization (DIN) exhibited negative responses. In lieu of developing specific thresholds for the management of nutrients as a stressor on coral reefs, we highlight important inflection points in the magnitude and direction of the effects of inorganic nutrients and identify trends among coral responses. The responses of corals to nutrients are complex, warranting conservative guidelines for elevated nutrient concentrations on coral reefs.

Effects of sediment exposure on corals: a systematic review of experimental studies.

BACKGROUND: Management actions that address local-scale stressors on coral reefs can rapidly improve water quality and reef ecosystem condition. In response to reef managers who need actionable thresholds for coastal runoff and dredging, we conducted a systematic review and meta-analysis of experimental studies that explore the effects of sediment on corals. We identified exposure levels that 'adversely' affect corals while accounting for sediment bearing (deposited vs. suspended), coral life-history stage, and species, thus providing empirically based estimates of stressor thresholds on vulnerable coral reefs. METHODS: We searched online databases and grey literature to obtain a list of potential studies, assess their eligibility, and critically appraise them for validity and risk of bias. Data were extracted from eligible studies and grouped by sediment bearing and coral response to identify thresholds in terms of the lowest exposure levels that induced an adverse physiological and/or lethal effect. Meta-regression estimated the dose-response relationship between exposure level and the magnitude of a coral's response, with random-effects structures to estimate the proportion of variance explained by factors such as study and coral species. REVIEW FINDINGS: After critical appraisal of over 15,000 records, our systematic review of corals' responses to sediment identified 86 studies to be included in meta-analyses (45 studies for deposited sediment and 42 studies for suspended sediment). The lowest sediment exposure levels that caused adverse effects in corals were well below the levels previously described as 'normal' on reefs: for deposited sediment, adverse effects occurred as low as 1 mg/cm2/day for larvae (limited settlement rates) and 4.9 mg/cm2/day for adults (tissue mortality); for suspended sediment, adverse effects occurred as low as 10 mg/L for juveniles (reduced growth rates) and 3.2 mg/L for adults (bleaching and tissue mortality). Corals take at least 10 times longer to experience tissue mortality from exposure to suspended sediment than to comparable concentrations of deposited sediment, though physiological changes manifest 10 times faster in response to suspended sediment than to deposited sediment. Threshold estimates derived from continuous response variables (magnitude of adverse effect) largely matched the lowest-observed adverse-effect levels from a summary of studies, or otherwise helped us to identify research gaps that should be addressed to better quantify the dose-response relationship between sediment exposure and coral health. CONCLUSIONS: We compiled a global dataset that spans three oceans, over 140 coral species, decades of research, and a range of field- and lab-based approaches. Our review and meta-analysis inform the no-observed and lowest-observed adverse-effect levels (NOAEL, LOAEL) that are used in management consultations by U.S. federal agencies. In the absence of more location- or species-specific data to inform decisions, our results provide the best available information to protect vulnerable reef-building corals from sediment stress. Based on gaps and limitations identified by our review, we make recommendations to improve future studies and recommend future synthesis to disentangle the potentially synergistic effects of multiple coral-reef stressors. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13750-022-00256-0.

Community similarity and species overlap between habitats provide insight into the deep reef refuge hypothesis.

The deep reef refuge hypothesis (DRRH) postulates that mesophotic coral ecosystems (MCEs) may provide a refuge for shallow coral reefs (SCRs). Understanding this process is an important conservation tool given increasing threats to coral reefs. To establish a better framework to analyze the DRRH, we analyzed stony coral communities in American Samoa across MCEs and SCRs to describe the community similarity and species overlap to test the foundational assumption of the DRRH. We suggest a different approach to determine species as depth specialists or generalists that changes the conceptual role of MCEs and emphasizes their importance in conservation planning regardless of their role as a refuge or not. This further encourages a reconsideration of a broader framework for the DRRH. We found 12 species of corals exclusively on MCEs and 183 exclusively on SCRs with another 63 species overlapping between depth zones. Of these, 19 appear to have the greatest potential to serve as reseeding species. Two additional species are listed under the U.S. Endangered Species Act, Acropora speciosa and Fimbriaphyllia paradivisa categorized as an occasional deep specialist and a deep exclusive species, respectively. Based on the community distinctiveness and minimal species overlap of SCR and MCE communities, we propose a broader framework by evaluating species overlap across coral reef habitats. This provides an opportunity to consider the opposite of the DRRH where SCRs support MCEs.

Coral reef biofilm bacterial diversity and successional trajectories are structured by reef benthic organisms and shift under chronic nutrient enrichment.

Work on marine biofilms has primarily focused on host-associated habitats for their roles in larval recruitment and disease dynamics; little is known about the factors regulating the composition of reef environmental biofilms. To contrast the roles of succession, benthic communities and nutrients in structuring marine biofilms, we surveyed bacteria communities in biofilms through a six-week succession in aquaria containing macroalgae, coral, or reef sand factorially crossed with three levels of continuous nutrient enrichment. Our findings demonstrate how biofilm successional trajectories diverge from temporal dynamics of the bacterioplankton and how biofilms are structured by the surrounding benthic organisms and nutrient enrichment. We identify a suite of biofilm-associated bacteria linked with the orthogonal influences of corals, algae and nutrients and distinct from the overlying water. Our results provide a comprehensive characterization of marine biofilm successional dynamics and contextualize the impact of widespread changes in reef community composition and nutrient pollution on biofilm community structure.

How phenological tracking shapes species and communities in non-stationary environments.

Climate change alters the environments of all species. Predicting species responses requires understanding how species track environmental change, and how such tracking shapes communities. Growing empirical evidence suggests that how species track phenologically - how an organism shifts the timing of major biological events in response to the environment - is linked to species performance and community structure. Such research tantalizingly suggests a potential framework to predict the winners and losers of climate change, and the future communities we can expect. But developing this framework requires far greater efforts to ground empirical studies of phenological tracking in relevant ecological theory. Here we review the concept of phenological tracking in empirical studies and through the lens of coexistence theory to show why a community-level perspective is critical to accurate predictions with climate change. While much current theory for tracking ignores the importance of a multi-species context, basic community assembly theory predicts that competition will drive variation in tracking and trade-offs with other traits. We highlight how existing community assembly theory can help understand tracking in stationary and non-stationary systems. But major advances in predicting the species- and community-level consequences of climate change will require advances in theoretical and empirical studies. We outline a path forward built on greater efforts to integrate priority effects into modern coexistence theory, improved empirical estimates of multivariate environmental change, and clearly defined estimates of phenological tracking and its underlying environmental cues.

Water quality thresholds for coastal contaminant impacts on corals: A systematic review and meta-analysis.

Reduced water quality degrades coral reefs, resulting in compromised ecosystem function and services to coastal communities. Increasing management capacity on reefs requires prioritization of the development of data-based water-quality thresholds and tipping points. To meet this urgent need of marine resource managers, we conducted a systematic review and meta-analysis that quantified the effects on scleractinian corals of chemical pollutants from land-based and atmospheric sources. We compiled a global dataset addressing the effects of these pollutants on coral growth, mortality, reproduction, physiology, and behavior. The resulting quantitative review of 55 articles includes information about industrial sources, modes of action, experimentally tested concentrations, and previously identified tolerance thresholds of corals to 13 metals, 18 pesticides, 5 polycyclic aromatic hydrocarbons (PAHs), a polychlorinated biphenyl (PCB), and a pharmaceutical. For data-rich contaminants, we make more robust threshold estimates by adapting models for Bayesian hierarchical meta-analysis that were originally developed for biopharmaceutical application. These models use information from multiple studies to characterize the dose-response relationships (i.e., Emax curves) between a pollutant's concentration and various measures of coral health. Metals used in antifouling paints, especially copper, have received a great deal of attention to-date, thus enabling us to estimate the cumulative impact of copper across coral's early life-history. The effects of other land-based pollutants on corals are comparatively understudied, which precludes more quantitative analysis. We discuss opportunities to improve future research so that it can be better integrated into quantitative assessments of the effects of more pollutant types on sublethal coral stress-responses. We also recommend that managers use this information to establish more conservative water quality thresholds that account for the synergistic effects of multiple pollutants on coral reefs. Ultimately, active remediation of local stressors will improve the resistance, resilience, and recovery of individual reefs and reef ecosystems facing the global threat of climate change.

Submarine groundwater discharge alters coral reef ecosystem metabolism.

Submarine groundwater discharge (SGD) influences near-shore coral reef ecosystems worldwide. SGD biogeochemistry is distinct, typically with higher nutrients, lower pH, cooler temperature and lower salinity than receiving waters. SGD can also be a conduit for anthropogenic nutrients and other pollutants. Using Bayesian structural equation modelling, we investigate pathways and feedbacks by which SGD influences coral reef ecosystem metabolism at two Hawai'i sites with distinct aquifer chemistry. The thermal and biogeochemical environment created by SGD changed net ecosystem production (NEP) and net ecosystem calcification (NEC). NEP showed a nonlinear relationship with SGD-enhanced nutrients: high fluxes of moderately enriched SGD (Wailupe low tide) and low fluxes of highly enriched SGD (Kupikipiki'o high tide) increased NEP, but high fluxes of highly enriched SGD (Kupikipiki'o low tide) decreased NEP, indicating a shift toward microbial respiration. pH fluctuated with NEP, driving changes in the net growth of calcifiers (NEC). SGD enhances biological feedbacks: changes in SGD from land use and climate change will have consequences for calcification of coral reef communities, and thereby shoreline protection.

Case-control design identifies ecological drivers of endemic coral diseases.

Endemic disease transmission is an important ecological process that is challenging to study because of low occurrence rates. Here, we investigate the ecological drivers of two coral diseases-growth anomalies and tissue loss-affecting five coral species. We first show that a statistical framework called the case-control study design, commonly used in epidemiology but rarely applied to ecology, provided high predictive accuracy (67-82%) and disease detection rates (60-83%) compared with a traditional statistical approach that yielded high accuracy (98-100%) but low disease detection rates (0-17%). Using this framework, we found evidence that 1) larger corals have higher disease risk; 2) shallow reefs with low herbivorous fish abundance, limited water motion, and located adjacent to watersheds with high fertilizer and pesticide runoff promote low levels of growth anomalies, a chronic coral disease; and 3) wave exposure, stream exposure, depth, and low thermal stress are associated with tissue loss disease risk during interepidemic periods. Variation in risk factors across host-disease pairs suggests that either different pathogens cause the same gross lesions in different species or that the same disease may arise in different species under different ecological conditions.

Divergent symbiont communities determine the physiology and nutrition of a reef coral across a light-availability gradient.

Reef corals are mixotrophic organisms relying on symbiont-derived photoautotrophy and water column heterotrophy. Coral endosymbionts (Family: Symbiodiniaceae), while typically considered mutualists, display a range of species-specific and environmentally mediated opportunism in their interactions with coral hosts, potentially requiring corals to rely more on heterotrophy to avoid declines in performance. To test the influence of symbiont communities on coral physiology (tissue biomass, symbiont density, photopigmentation) and nutrition (δ13C, δ15N), we sampled Montipora capitata colonies dominated by a specialist symbiont Cladocopium spp. or a putative opportunist Durusdinium glynnii (hereafter, C- or D-colonies) from Kane'ohe Bay, Hawai'i, across gradients in photosynthetically active radiation (PAR) during summer and winter. We report for the first time that isotope values of reef corals are influenced by Symbiodiniaceae communities, indicative of different autotrophic capacities among symbiont species. D-colonies had on average 56% higher symbiont densities, but lower photopigments per symbiont cell and consistently lower δ13C values in host and symbiont tissues; this pattern in isotope values is consistent with lower symbiont carbon assimilation and translocation to the host. Neither C- nor D-colonies showed signs of greater heterotrophy or nutritional plasticity; instead changes in δ13C values were driven by PAR availability and photoacclimation attributes that differed between symbiont communities. Together, these results reveal Symbiodiniaceae functional diversity produces distinct holobionts with different capacities for autotrophic nutrition, and energy tradeoffs from associating with opportunist symbionts are not met with increased heterotrophy.

CoralCam: A flexible, low-cost ecological monitoring platform.

The study and conservation of biological communities, such as coral reefs, frequently requires repeated surveys to measure the growth of organisms or the occurrence of ecological processes, such as recruitment, predation, competition, or mortality. In the case of coral reefs, processes influencing coral community structure occur on time scales of days (recruitment, predation), months (seasonal environmental stress), or years (competition for space). In both marine and terrestrial systems, observing the ecology of remote locations at fine temporal scales is made difficult by the high cost or complexity of resurveying the same location at high frequency. These restrictions have produced limited understanding of in-situ ecological processes which occur at fine temporal scales and influence community structure but are easily missed during infrequent surveys. We present a low-cost method for the conversion of consumer cameras into programmable time-lapse platforms, allowing scheduled daily video or photo capture in remote locations for extended time periods. Results of a 1-month deployment with twice-daily photo capture are presented. Total cost to construct and deploy CoralCam in-situ (up to 45 m) is approximately $80 USD, providing a low-cost platform for fine scale data collection where these data are not otherwise logistically or financially possible.

Nutrient pollution disrupts key ecosystem functions on coral reefs.

There is a long history of examining the impacts of nutrient pollution and pH on coral reefs. However, little is known about how these two stressors interact and influence coral reef ecosystem functioning. Using a six-week nutrient addition experiment, we measured the impact of elevated nitrate (NO-3) and phosphate (PO3-4) on net community calcification (NCC) and net community production (NCP) rates of individual taxa and combined reef communities. Our study had four major outcomes: (i) NCC rates declined in response to nutrient addition in all substrate types, (ii) the mixed community switched from net calcification to net dissolution under medium and high nutrient conditions, (iii) nutrients augmented pH variability through modified photosynthesis and respiration rates, and (iv) nutrients disrupted the relationship between NCC and aragonite saturation state documented in ambient conditions. These results indicate that the negative effect of NO-3 and PO3-4 addition on reef calcification is likely both a direct physiological response to nutrients and also an indirect response to a shifting pH environment from altered NCP rates. Here, we show that nutrient pollution could make reefs more vulnerable to global changes associated with ocean acidification and accelerate the predicted shift from net accretion to net erosion.

Host size and proximity to diseased neighbours drive the spread of a coral disease outbreak in Hawai'i.

Understanding how disease risk varies over time and across heterogeneous populations is critical for managing disease outbreaks, but this information is rarely known for wildlife diseases. Here, we demonstrate that variation in host and pathogen factors drive the direction, duration and intensity of a coral disease outbreak. We collected longitudinal health data for 200 coral colonies, and found that disease risk increased with host size and severity of diseased neighbours, and disease spread was highest among individuals between 5 and 20 m apart. Disease risk increased by 2% with every 10 cm increase in host size. Healthy colonies with severely diseased neighbours (greater than 75% affected tissue) were 1.6 times more likely to develop disease signs compared with colonies with moderately diseased neighbours (25-75% affected tissue). Force of infection ranged from 7 to 20 disease cases per 1000 colonies (mean = 15 cases per 1000 colonies). The effective reproductive ratio, or average number of secondary infections per infectious individual, ranged from 0.16 to 1.22. Probability of transmission depended strongly on proximity to diseased neighbours, which demonstrates that marine disease spread can be highly constrained within patch reefs.

Environmental drivers of coral reef carbonate production and bioerosion: a multi-scale analysis.

The resilience of coral reefs depends on the balance between reef growth and reef breakdown, and their responses to changing environmental conditions. Across the 2500-km Hawaiian Archipelago, we quantified rates of carbonate production, bioerosion, and net accretion at regional, island, site, and within-site spatial scales and tested how these rates respond to environmental conditions across different spatial scales. Overall, there were four major outcomes from this study: (1) bioerosion rates were generally higher in the populated Main Hawaiian Islands (MHI) than the remote, protected Northwestern Hawaiian Islands (NWHI), while carbonate production rates did not vary significantly between the two regions; (2) variability in carbonate production, bioerosion, and net accretion rates was greatest at the smallest within-reef spatial scale; (3) carbonate production and bioerosion rates were associated with distinct sets of environmental parameters; and (4) the strongest correlates of carbonate production, bioerosion, and net accretion rates were different between the MHI region and the NWHI region: in the MHI, the dominant correlates were percent cover of macroalgae and herbivorous fish biomass for carbonate production and bioerosion, respectively, whereas in the NWHI, the top correlates were total alkalinity and benthic cover. This study highlights the need to understand accretion and erosion processes as well as local environmental conditions to predict net coral reef responses to future environmental changes.

A Novel µCT Analysis Reveals Different Responses of Bioerosion and Secondary Accretion to Environmental Variability.

Corals build reefs through accretion of calcium carbonate (CaCO3) skeletons, but net reef growth also depends on bioerosion by grazers and borers and on secondary calcification by crustose coralline algae and other calcifying invertebrates. However, traditional field methods for quantifying secondary accretion and bioerosion confound both processes, do not measure them on the same time-scale, or are restricted to 2D methods. In a prior study, we compared multiple environmental drivers of net erosion using pre- and post-deployment micro-computed tomography scans (µCT; calculated as the % change in volume of experimental CaCO3 blocks) and found a shift from net accretion to net erosion with increasing ocean acidity. Here, we present a novel µCT method and detail a procedure that aligns and digitally subtracts pre- and post-deployment µCT scans and measures the simultaneous response of secondary accretion and bioerosion on blocks exposed to the same environmental variation over the same time-scale. We tested our method on a dataset from a prior study and show that it can be used to uncover information previously unattainable using traditional methods. We demonstrated that secondary accretion and bioerosion are driven by different environmental parameters, bioerosion is more sensitive to ocean acidity than secondary accretion, and net erosion is driven more by changes in bioerosion than secondary accretion.

Satellite SST-Based Coral Disease Outbreak Predictions for the Hawaiian Archipelago.

Predicting wildlife disease risk is essential for effective monitoring and management, especially for geographically expansive ecosystems such as coral reefs in the Hawaiian archipelago. Warming ocean temperature has increased coral disease outbreaks contributing to declines in coral cover worldwide. In this study we investigated seasonal effects of thermal stress on the prevalence of the three most widespread coral diseases in Hawai'i: Montipora white syndrome, Porites growth anomalies and Porites tissue loss syndrome. To predict outbreak likelihood we compared disease prevalence from surveys conducted between 2004 and 2015 from 18 Hawaiian Islands and atolls with biotic (e.g., coral density) and abiotic (satellite-derived sea surface temperature metrics) variables using boosted regression trees. To date, the only coral disease forecast models available were developed for Acropora white syndrome on the Great Barrier Reef (GBR). Given the complexities of disease etiology, differences in host demography and environmental conditions across reef regions, it is important to refine and adapt such models for different diseases and geographic regions of interest. Similar to the Acropora white syndrome models, anomalously warm conditions were important for predicting Montipora white syndrome, possibly due to a relationship between thermal stress and a compromised host immune system. However, coral density and winter conditions were the most important predictors of all three coral diseases in this study, enabling development of a forecasting system that can predict regions of elevated disease risk up to six months before an expected outbreak. Our research indicates satellite-derived systems for forecasting disease outbreaks can be appropriately adapted from the GBR tools and applied for a variety of diseases in a new region. These models can be used to enhance management capacity to prepare for and respond to emerging coral diseases throughout Hawai'i and can be modified for other diseases and regions around the world.

Location Isn't Everything: Timing of Spawning Aggregations Optimizes Larval Replenishment.

Many species of reef fishes form large spawning aggregations that are highly predictable in space and time. Prior research has suggested that aggregating fish derive fitness benefits not just from mating at high density but, also, from oceanographic features of the spatial locations where aggregations occur. Using a probabilistic biophysical model of larval dispersal coupled to a fine resolution hydrodynamic model of the Florida Straits, we develop a stochastic landscape of larval fitness. Tracking virtual larvae from release to settlement and incorporating changes in larval behavior through ontogeny, we found that larval success was sensitive to the timing of spawning. Indeed, propagules released during the observed spawning period had higher larval success rates than those released outside the observed spawning period. In contrast, larval success rates were relatively insensitive to the spatial position of the release site. In addition, minimum (rather than mean) larval survival was maximized during the observed spawning period, indicating a reproductive strategy that minimizes the probability of recruitment failure. Given this landscape of larval fitness, we take an inverse optimization approach to define a biological objective function that reflects a tradeoff between the mean and variance of larval success in a temporally variable environment. Using this objective function, we suggest that the length of the spawning period can provide insight into the tradeoff between reproductive risk and reward.