Errors in estimating reproductive parameters with macroscopic methods: a case study on the protogynous blacktip grouper Epinephelus fasciatus (Forsskål 1775).

A size-based, histological analysis of the reproductive life history of the blacktip grouper, Epinephelus fasciatus (Forsskål 1775), was conducted in Indonesia to evaluate the error rate associated with macroscopic reproductive analysis. Histological results indicated that E. fasciatus was protogynous with female L50 at 13.4 cm total length (LT) and a size at sexual transition of 22.0 cm LT. The weight-length relationship for the species was W = 0.011 L3.13. Overall sex ratios were significantly female biased, operational sex ratios were significantly male biased, and sex ratios of mature individuals varied predictably with length from female to male dominance as size increased. No significant relationship between length and batch fecundity was found. The population has a spawning period from February to August. Overall, 54.4% of macroscopic evaluations were incorrect compared to histological results. Of the errors, 14.8% were a failure to detect ovotestes, 12.7% were classifying non-gonadal tissue as ovary or testis, 12.2% were misclassifying sex, and 12.7% were misclassifying maturity status. However, the largest source of error (47.7%) was from misclassifying both sex and maturity status. Of these, 92.9% were macroscopically classified as immature females, but were histologically confirmed to be mature males. Compared to histological results, the only accurate macroscopic results were the absence of a sex-based difference in weight-length relationship and spawning seasonality estimated by a gonadosomatic index (February-June). The use of macroscopic methods to estimate reproductive life-history parameters for sex-changing reefes fish may introduce significant inaccuracies and misinterpretations. Of the parameters estimated by histological methods, size at maturity, size-specific sex ratios, and spawning seasonality have the greatest potential to inform local fishery management policy.

Increased occurrence of the rare golden color morph of Pacific chub Kyphosus sandwicensis in a no-take marine reserve.

Pacific chub, Kyphosus sandwicensis, are typically gray but some individuals display a golden color morph. We estimated that the frequency of occurrence of the golden morphs increased significantly from 2007 (1.9%) and 2012 (2.6%) to 2017 (5.0%) inside a no-take marine reserve around Nihoa Island in the Northwestern Hawaiian Islands. While sporadic observations of a golden color morph have been noted for several other marine fish species, we provide a quantitative estimate of changes in the frequency of occurrence of the morph within a wild marine population.

Co-occurring anthropogenic stressors reduce the timeframe of environmental viability for the world's coral reefs.

Anthropogenic disturbances are posing unprecedented challenges to the persistence of ecosystems worldwide. The speed at which these disturbances reach an ecosystem's tolerance thresholds will determine the time available for adaptation and conservation. Here, we aim to calculate the year after which a given environmental stressor permanently exceeds the bounds of an ecosystem's tolerance. Ecosystem thresholds are here defined as limits in a given stressor beyond which ecosystems have showed considerable changes in community assembly and functioning, becoming remnants of what they once were, but not necessarily leading to species extirpation or extinction. Using the world's coral reefs as a case example, we show that the projected effects of marine heatwaves, ocean acidification, storms, land-based pollution, and local human stressors are being underestimated considerably by looking at disturbances independently. Given the spatial complementarity in which numerous disturbances impact the world's coral reefs, we show that the timelines of environmental suitability are halved when all disturbances are analyzed simultaneously, as opposed to independently. Under business-as-usual scenarios, the median year after which environmental conditions become unsuitable for the world's remaining coral reefs was, at worse, 2050 for any one disturbance alone (28 years left); but when analyzed concurrently, this date was shortened to 2035 (13 years left). When analyzed together, disturbances reduced the date of environmental suitability because areas that may remain suitable under one disturbance could become unsuitable by any of several other variables. The significance of co-occurring disturbances at reducing timeframes of environmental suitability was evident even under optimistic scenarios. The best-case scenario, characterized by strong mitigation of greenhouse gas emissions and optimistic human development, resulted in 41% of global coral reefs with unsuitable conditions by 2100 under any one disturbance independently; yet when analyzed in combination up to 64% of the world's coral reefs could face unsuitable environmental conditions by one disturbance or another. Under the worst-case scenario, nearly all coral reef ecosystems worldwide (approximately 99%) will permanently face unsuitable conditions by 2055 in at least one of the disturbances analyzed. Prior studies have indicated the projected dire effects of climate change on coral reefs by mid-century; by analyzing a multitude of projected disturbances, our study reveals a much more severe prognosis for the world's coral reefs as they have significantly less time to adapt while highlighting the urgent need to tackle available solutions to human disturbances.

Over half of known human pathogenic diseases can be aggravated by climate change.

It is relatively well accepted that climate change can affect human pathogenic diseases; however, the full extent of this risk remains poorly quantified. Here we carried out a systematic search for empirical examples about the impacts of ten climatic hazards sensitive to greenhouse gas (GHG) emissions on each known human pathogenic disease. We found that 58% (that is, 218 out of 375) of infectious diseases confronted by humanity worldwide have been at some point aggravated by climatic hazards; 16% were at times diminished. Empirical cases revealed 1,006 unique pathways in which climatic hazards, via different transmission types, led to pathogenic diseases. The human pathogenic diseases and transmission pathways aggravated by climatic hazards are too numerous for comprehensive societal adaptations, highlighting the urgent need to work at the source of the problem: reducing GHG emissions.

No butts about it: using urogenital disparity in a deep-water snapper, Etelis carbunculus (Lutjanidae), for field-based sexual identification.

In this study, the authors describe a process that consistently identified sex based on differences in the length and characteristics of the urogenital papilla septum of Etelis carbunculus, a deep-water snapper (Lutjanidae, Etelinae). These characteristics, regardless of fish size, were found to be accurate for 96% of 157 specimens evaluated. The application of this external sex determination technique expedites the collection of sex-specific data and may perform well for other morphologically similar lutjanid snappers. The non-invasive method also minimizes damage to the fish, thereby allowing either its return to the ocean or landing as a valuable whole fish.

Social-environmental drivers inform strategic management of coral reefs in the Anthropocene.

Without drastic efforts to reduce carbon emissions and mitigate globalized stressors, tropical coral reefs are in jeopardy. Strategic conservation and management requires identification of the environmental and socioeconomic factors driving the persistence of scleractinian coral assemblages-the foundation species of coral reef ecosystems. Here, we compiled coral abundance data from 2,584 Indo-Pacific reefs to evaluate the influence of 21 climate, social and environmental drivers on the ecology of reef coral assemblages. Higher abundances of framework-building corals were typically associated with: weaker thermal disturbances and longer intervals for potential recovery; slower human population growth; reduced access by human settlements and markets; and less nearby agriculture. We therefore propose a framework of three management strategies (protect, recover or transform) by considering: (1) if reefs were above or below a proposed threshold of >10% cover of the coral taxa important for structural complexity and carbonate production; and (2) reef exposure to severe thermal stress during the 2014-2017 global coral bleaching event. Our findings can guide urgent management efforts for coral reefs, by identifying key threats across multiple scales and strategic policy priorities that might sustain a network of functioning reefs in the Indo-Pacific to avoid ecosystem collapse.

Corrigendum: The Coral Trait Database, a curated database of trait information for coral species from the global oceans.

This corrects the article DOI: 10.1038/sdata.2016.17.

The implementation of rare events logistic regression to predict the distribution of mesophotic hard corals across the main Hawaiian Islands.

Predictive habitat suitability models are powerful tools for cost-effective, statistically robust assessment of the environmental drivers of species distributions. The aim of this study was to develop predictive habitat suitability models for two genera of scleractinian corals (Leptoserisand Montipora) found within the mesophotic zone across the main Hawaiian Islands. The mesophotic zone (30-180 m) is challenging to reach, and therefore historically understudied, because it falls between the maximum limit of SCUBA divers and the minimum typical working depth of submersible vehicles. Here, we implement a logistic regression with rare events corrections to account for the scarcity of presence observations within the dataset. These corrections reduced the coefficient error and improved overall prediction success (73.6% and 74.3%) for both original regression models. The final models included depth, rugosity, slope, mean current velocity, and wave height as the best environmental covariates for predicting the occurrence of the two genera in the mesophotic zone. Using an objectively selected theta ("presence") threshold, the predicted presence probability values (average of 0.051 for Leptoseris and 0.040 for Montipora) were translated to spatially-explicit habitat suitability maps of the main Hawaiian Islands at 25 m grid cell resolution. Our maps are the first of their kind to use extant presence and absence data to examine the habitat preferences of these two dominant mesophotic coral genera across Hawai'i.

The Coral Trait Database, a curated database of trait information for coral species from the global oceans.

Trait-based approaches advance ecological and evolutionary research because traits provide a strong link to an organism's function and fitness. Trait-based research might lead to a deeper understanding of the functions of, and services provided by, ecosystems, thereby improving management, which is vital in the current era of rapid environmental change. Coral reef scientists have long collected trait data for corals; however, these are difficult to access and often under-utilized in addressing large-scale questions. We present the Coral Trait Database initiative that aims to bring together physiological, morphological, ecological, phylogenetic and biogeographic trait information into a single repository. The database houses species- and individual-level data from published field and experimental studies alongside contextual data that provide important framing for analyses. In this data descriptor, we release data for 56 traits for 1547 species, and present a collaborative platform on which other trait data are being actively federated. Our overall goal is for the Coral Trait Database to become an open-source, community-led data clearinghouse that accelerates coral reef research.

Persistence and change in community composition of reef corals through present, past, and future climates.

The reduction in coral cover on many contemporary tropical reefs suggests a different set of coral community assemblages will dominate future reefs. To evaluate the capacity of reef corals to persist over various time scales, we examined coral community dynamics in contemporary, fossil, and simulated future coral reef ecosystems. Based on studies between 1987 and 2012 at two locations in the Caribbean, and between 1981 and 2013 at five locations in the Indo-Pacific, we show that many coral genera declined in abundance, some showed no change in abundance, and a few coral genera increased in abundance. Whether the abundance of a genus declined, increased, or was conserved, was independent of coral family. An analysis of fossil-reef communities in the Caribbean revealed changes in numerical dominance and relative abundances of coral genera, and demonstrated that neither dominance nor taxon was associated with persistence. As coral family was a poor predictor of performance on contemporary reefs, a trait-based, dynamic, multi-patch model was developed to explore the phenotypic basis of ecological performance in a warmer future. Sensitivity analyses revealed that upon exposure to thermal stress, thermal tolerance, growth rate, and longevity were the most important predictors of coral persistence. Together, our results underscore the high variation in the rates and direction of change in coral abundances on contemporary and fossil reefs. Given this variation, it remains possible that coral reefs will be populated by a subset of the present coral fauna in a future that is warmer than the recent past.

Between tide and wave marks: a unifying model of physical zonation on littoral shores.

The effects of tides on littoral marine habitats are so ubiquitous that shorelines are commonly described as 'intertidal', whereas waves are considered a secondary factor that simply modifies the intertidal habitat. However mean significant wave height exceeds tidal range at many locations worldwide. Here we construct a simple sinusoidal model of coastal water level based on both tidal range and wave height. From the patterns of emergence and submergence predicted by the model, we derive four vertical shoreline benchmarks which bracket up to three novel, spatially distinct, and physically defined zones. The (1) emergent tidal zone is characterized by tidally driven emergence in air; the (2) wave zone is characterized by constant (not periodic) wave wash; and the (3) submergent tidal zone is characterized by tidally driven submergence. The decoupling of tidally driven emergence and submergence made possible by wave action is a critical prediction of the model. On wave-dominated shores (wave height ≫ tidal range), all three zones are predicted to exist separately, but on tide-dominated shores (tidal range ≫ wave height) the wave zone is absent and the emergent and submergent tidal zones overlap substantially, forming the traditional "intertidal zone". We conclude by incorporating time and space in the model to illustrate variability in the physical conditions and zonation on littoral shores. The wave:tide physical zonation model is a unifying framework that can facilitate our understanding of physical conditions on littoral shores whether tropical or temperate, marine or lentic.

Symbiotic specificity, association patterns, and function determine community responses to global changes: defining critical research areas for coral-Symbiodinium symbioses.

Climate change-driven stressors threaten the persistence of coral reefs worldwide. Symbiotic relationships between scleractinian corals and photosynthetic endosymbionts (genus Symbiodinium) are the foundation of reef ecosystems, and these associations are differentially impacted by stress. Here, we couple empirical data from the coral reefs of Moorea, French Polynesia, and a network theoretic modeling approach to evaluate how patterns in coral-Symbiodinium associations influence community stability under climate change. To introduce the effect of climate perturbations, we simulate local 'extinctions' that represent either the loss of coral species or the ability to engage in symbiotic interactions. Community stability is measured by determining the duration and number of species that persist through the simulated extinctions. Our results suggest that four factors greatly increase coral-Symbiodinium community stability in response to global changes: (i) the survival of generalist hosts and symbionts maximizes potential symbiotic unions; (ii) elevated symbiont diversity provides redundant or complementary symbiotic functions; (iii) compatible symbiotic assemblages create the potential for local recolonization; and (iv) the persistence of certain traits associate with symbiotic diversity and redundancy. Symbiodinium may facilitate coral persistence through novel environmental regimes, but this capacity is mediated by symbiotic specificity, association patterns, and the functional performance of the symbionts. Our model-based approach identifies general trends and testable hypotheses in coral-Symbiodinium community responses. Future studies should consider similar methods when community size and/or environmental complexity preclude experimental approaches.

The distribution of the thermally tolerant symbiont lineage (Symbiodinium clade D) in corals from Hawaii: correlations with host and the history of ocean thermal stress.

Spatially intimate symbioses, such as those between scleractinian corals and unicellular algae belonging to the genus Symbiodinium, can potentially adapt to changes in the environment by altering the taxonomic composition of their endosymbiont communities. We quantified the spatial relationship between the cumulative frequency of thermal stress anomalies (TSAs) and the taxonomic composition of Symbiodinium in the corals Montipora capitata, Porites lobata, and Porites compressa across the Hawaiian archipelago. Specifically, we investigated whether thermally tolerant clade D Symbiodinium was in greater abundance in corals from sites with high frequencies of TSAs. We recovered 2305 Symbiodinium ITS2 sequences from 242 coral colonies in lagoonal reef habitats at Pearl and Hermes Atoll, French Frigate Shoals, and Kaneohe Bay, Oahu in 2007. Sequences were grouped into 26 operational taxonomic units (OTUs) with 12 OTUs associated with Montipora and 21 with Porites. Both coral genera associated with Symbiodinium in clade C, and these co-occurred with clade D in M. capitata and clade G in P. lobata. The latter represents the first report of clade G Symbiodinium in P. lobata. In M. capitata (but not Porites spp.), there was a significant correlation between the presence of Symbiodinium in clade D and a thermal history characterized by high cumulative frequency of TSAs. The endogenous community composition of Symbiodinium and an association with clade D symbionts after long-term thermal disturbance appear strongly dependent on the taxa of the coral host.

Methods for assessment of short-term coral reef fish movements within an acoustic array.

BACKGROUND: Arrays of passive receivers are a widely used tool for tracking the movements of acoustically-tagged fish in marine ecosystems; however, the spatial and temporal heterogeneity of coral reef environments pose challenges for the interpretation of tag detection data. To improve this situation for reef fishes, we introduced a novel response variable method that treats signal detections as proportions (i.e., percent transmissions detected or "detection rates") and compared this against prior approaches to examine the influence of array and transmitter performance, signal distance and environmental factors on detection rates. We applied this method to tagged snappers and groupers in the Florida reef ecosystem and controlled range-tests on static targets in Bayboro Harbor, Florida, to provide methodological guidance for the planning and evaluation of passive array studies for coral reef fishes. RESULTS: Logistic regression analysis indicated detection rates were primarily a non-linear function of tag distance from receiver. A 'model-weighted' function was developed to incorporate the non-linear relationship between detection rate and distance to provide robust positioning estimates and allow for easy extension to tags with different ping rates. CONCLUSIONS: Optimal acoustic array design requires balancing the interplay between receiver spacing, detection rates, and positioning error. Spacing receivers at twice the distance of the modeled 50% detection rate may be appropriate when quantification of overall space use is a priority, and would provide a minimum of 75% detection rate. However, for research where missing detections within the array is unacceptable or time-at-arrival based fine-scale positioning is needed, tighter receiver spacing may be required to maintain signal detection probability near 100%.

Transmission mode predicts specificity and interaction patterns in coral-Symbiodinium networks.

Most reef-building corals in the order Scleractinia depend on endosymbiotic algae in the genus Symbiodinium for energy and survival. Significant levels of taxonomic diversity in both partners result in numerous possible combinations of coral-Symbiodinium associations with unique functional characteristics. We created and analyzed the first coral-Symbiodinium networks utilizing a global dataset of interaction records from coral reefs in the tropical Indo-Pacific and Atlantic Oceans for 1991 to 2010. Our meta-analysis reveals that the majority of coral species and Symbiodinium types are specialists, but failed to detect any one-to-one obligate relationships. Symbiont specificity is correlated with a host's transmission mode, with horizontally transmitting corals being more likely to interact with generalist symbionts. Globally, Symbiodinium types tend to interact with only vertically or horizontally transmitting corals, and only a few generalist types are found with both. Our results demonstrate a strong correlation between symbiont specificity, symbiont transmission mode, and community partitioning. The structure and dynamics of these network interactions underlie the fundamental biological partnership that determines the condition and resilience of coral reef ecosystems.

Hosts of the Plio-Pleistocene past reflect modern-day coral vulnerability.

The risk of global extinction of reef-building coral species is increasing. We evaluated extinction risk using a biological trait-based resiliency index that was compared with Caribbean extinction during the Plio-Pleistocene, and with extinction risk determined by the International Union for Conservation of Nature (IUCN). Through the Plio-Pleistocene, the Caribbean supported more diverse coral assemblages than today and shared considerable overlap with contemporary Indo-Pacific reefs. A clear association was found between extant Plio-Pleistocene coral genera and our positive resilience scores. Regional extinction in the past and vulnerability in the present suggests that Pocillopora, Stylophora and foliose Pavona are among the most susceptible taxa to local and regional isolation. These same taxa were among the most abundant corals in the Caribbean Pliocene. Therefore, a widespread distribution did not equate with immunity to regional extinction. The strong relationship between past and present vulnerability suggests that regional extinction events are trait-based and not merely random episodes. We found several inconsistencies between our data and the IUCN scores, which suggest a need to critically re-examine what constitutes coral vulnerability.

GeoSymbio: a hybrid, cloud-based web application of global geospatial bioinformatics and ecoinformatics for Symbiodinium-host symbioses.

The genus Symbiodinium encompasses a group of unicellular, photosynthetic dinoflagellates that are found free living or in hospite with a wide range of marine invertebrate hosts including scleractinian corals. We present GeoSymbio, a hybrid web application that provides an online, easy to use and freely accessible interface for users to discover, explore and utilize global geospatial bioinformatic and ecoinformatic data on Symbiodinium-host symbioses. The novelty of this application lies in the combination of a variety of query and visualization tools, including dynamic searchable maps, data tables with filter and grouping functions, and interactive charts that summarize the data. Importantly, this application is hosted remotely or 'in the cloud' using Google Apps, and therefore does not require any specialty GIS, web programming or data programming expertise from the user. The current version of the application utilizes Symbiodinium data based on the ITS2 genetic marker from PCR-based techniques, including denaturing gradient gel electrophoresis, sequencing and cloning of specimens collected during 1982-2010. All data elements of the application are also downloadable as spatial files, tables and nucleic acid sequence files in common formats for desktop analysis. The application provides a unique tool set to facilitate research on the basic biology of Symbiodinium and expedite new insights into their ecology, biogeography and evolution in the face of a changing global climate. GeoSymbio can be accessed at https://sites.google.com/site/geosymbio/.

Patterns of coral disease across the Hawaiian archipelago: relating disease to environment.

In Hawaii, coral reefs occur across a gradient of biological (host abundance), climatic (sea surface temperature anomalies) and anthropogenic conditions from the human-impacted reefs of the main Hawaiian Islands (MHI) to the pristine reefs of the northwestern Hawaiian Islands (NWHI). Coral disease surveys were conducted at 142 sites from across the Archipelago and disease patterns examined. Twelve diseases were recorded from three coral genera (Porites, Montipora, Acropora) with Porites having the highest prevalence. Porites growth anomalies (PorGAs) were significantly more prevalent within and indicative of reefs in the MHI and Porites trematodiasis (PorTrm) was significantly more prevalent within and indicative of reefs in the NWHI. Porites tissue loss syndrome (PorTLS) was also important in driving regional differences but that relationship was less clear. These results highlight the importance of understanding disease ecology when interpreting patterns of disease occurrence. PorTrm is caused by a parasitic flatworm that utilizes multiple hosts during its life cycle (fish, mollusk and coral). All three hosts must be present for the disease to occur and higher host abundance leads to higher disease prevalence. Thus, a high prevalence of PorTrm on Hawaiian reefs would be an indicator of a healthy coral reef ecosystem. In contrast, the high occurrence of PorGAs within the MHI suggests that PorGAs are related, directly or indirectly, to some environmental co-factor associated with increased human population sizes. Focusing on the three indicator diseases (PorGAs, PorTrm, PorTLS) we used statistical modeling to examine the underlying associations between disease prevalence and 14 different predictor variables (biotic and abiotic). All three diseases showed positive associations with host abundance and negative associations with thermal stress. The association with human population density differed among disease states with PorGAs showing a positive and PorTrm showing a negative association, but no significant explanatory power was offered for PorTLS.

Growth anomalies on the coral genera Acropora and Porites are strongly associated with host density and human population size across the Indo-Pacific.

Growth anomalies (GAs) are common, tumor-like diseases that can cause significant morbidity and decreased fecundity in the major Indo-Pacific reef-building coral genera, Acropora and Porites. GAs are unusually tractable for testing hypotheses about drivers of coral disease because of their pan-Pacific distributions, relatively high occurrence, and unambiguous ease of identification. We modeled multiple disease-environment associations that may underlie the prevalence of Acropora growth anomalies (AGA) (n = 304 surveys) and Porites growth anomalies (PGA) (n = 602 surveys) from across the Indo-Pacific. Nine predictor variables were modeled, including coral host abundance, human population size, and sea surface temperature and ultra-violet radiation anomalies. Prevalence of both AGAs and PGAs were strongly host density-dependent. PGAs additionally showed strong positive associations with human population size. Although this association has been widely posited, this is one of the first broad-scale studies unambiguously linking a coral disease with human population size. These results emphasize that individual coral diseases can show relatively distinct patterns of association with environmental predictors, even in similar diseases (growth anomalies) found on different host genera (Acropora vs. Porites). As human densities and environmental degradation increase globally, the prevalence of coral diseases like PGAs could increase accordingly, halted only perhaps by declines in host density below thresholds required for disease establishment.