Thresholds and drivers of coral calcification responses to climate change.

Increased temperature and CO2 levels are considered key drivers of coral reef degradation. However, individual assessments of ecological responses (calcification) to these stressors are often contradicting. To detect underlying drivers of heterogeneity in coral calcification responses, we developed a procedure for the inclusion of stress-effect relationships in ecological meta-analyses. We applied this technique to a dataset of 294 empirical observations from 62 peer-reviewed publications testing individual and combined effects of elevated temperature and pCO2 on coral calcification. Our results show an additive interaction between warming and acidification, which reduces coral calcification by 20% when pCO2 levels exceed 700 ppm and temperature increases by 3°C. However, stress levels varied among studies and significantly affected outcomes, with unaffected calcification rates under moderate stresses (pCO2  ≤ 700 ppm, ΔT < 3°C). Future coral reef carbon budgets will therefore depend on the magnitude of pCO2 and temperature elevations and, thus, anthropogenic CO2 emissions. Accounting for stress-effect relationships enabled us to identify additional drivers of heterogeneity including coral taxa, life stage, habitat, food availability, climate, and season. These differences can aid reef management identifying refuges and conservation priorities, but without a global effort to reduce CO2 emissions, coral capacity to build reefs will be at risk.

Comparative toxicity of hydrocarbons for evaluation of Lysmata boggessi as an experimental proxy for deep-water column micronekton.

The potential impacts of sub-surface hydrocarbon plumes to deep-water column micronekton are an important consideration in a more complete understanding of ecosystem effects resulting from deep-sea oil spills. However, evaluating toxicity in these organisms presents multiple challenges, and the use of a shallow-water proxy species allows comparison and validation of experimental results. This study thus examined the suitability of the peppermint shrimp, Lysmata boggessi, as an experimental proxy for ecologically important deep-sea zooplankton/micronekton in hydrocarbon toxicity assays. This crustacean species occurs in shallow coastal marine environments throughout the western Atlantic, Caribbean and Gulf of Mexico, is similar in size to the mesopelagic organisms previously tested and is readily available via commercial aquaculture. The effects of 1-methylnaphthalene and fresh Macondo oil (MC252) on L. boggessi were assessed in 48-h constant-exposure toxicity tests, and acute thresholds were compared to previously determined LC50s for oceanic mid water Euphausiidae, Janicella spinacauda, Systellaspis debilis, Sergestes sp., Sergia sp. and the mysid shrimp Americamysis bahia. Acute thresholds and the calculated critical target lipid body burden (CTLBB) for the shallow-water L. boggessi were comparable to the deep-water species tested, suggesting that L. boggessi may be a suitable proxy for some mesopelagic micronekton species in acute hydrocarbon exposures.

Climate and the latitudinal limits of subtropical reef development.

Climate plays a central role in coral-reef development, especially in marginal environments. The high-latitude reefs of southeast Florida are currently non-accreting, relict systems with low coral cover. This region also did not support the extensive Late Pleistocene reef development observed in many other locations around the world; however, there is evidence of significant reef building in southeast Florida during the Holocene. Using 146 radiometric ages from reefs extending ~ 120 km along Florida's southeast coast, we test the hypothesis that the latitudinal extent of Holocene reef development in this region was modulated by climatic variability. We demonstrate that although sea-level changes impacted rates of reef accretion and allowed reefs to backstep inshore as new habitats were flooded, sea level was not the ultimate cause of reef demise. Instead, we conclude that climate was the primary driver of the expansion and contraction of Florida's reefs during the Holocene. Reefs grew to 26.7° N in southeast Florida during the relatively warm, stable climate at the beginning of the Holocene Thermal Maximum (HTM) ~ 10,000 years ago, but subsequent cooling and increased frequency of winter cold fronts were associated with the equatorward contraction of reef building. By ~ 7800 years ago, actively accreting reefs only extended to 26.1° N. Reefs further contracted to 25.8° N after 5800 years ago, and by 3000 years ago reef development had terminated throughout southern Florida (24.5-26.7° N). Modern warming is unlikely to simply reverse this trend, however, because the climate of the Anthropocene will be fundamentally different from the HTM. By increasing the frequency and intensity of both warm and cold extreme-weather events, contemporary climate change will instead amplify conditions inimical to reef development in marginal reef environments such as southern Florida, making them more likely to continue to deteriorate than to resume accretion in the future.

Population dynamics of the reef crisis: Consequences of the growing human population.

An unequivocal link exists between human population density and environmental degradation, both in the near field (local impacts) and far field (impacts due to teleconnections). Human population is most widely predicted to reach 9-11 billion by 2100, when the demographic transition is expected in all but a handful of countries. Strongest population growth is in the tropics, where coral reefs face dense human population and concomitant heavy usage. In most countries, >50% will be urbanized but growth of rural population and need for food in urban centres will not alleviate pressure on reef resources. Aquaculture will alleviate some fishing pressure, but still utilizes reef surface and is also destructive. Denser coastal populations and greater wealth will lead to reef degradation by coastal construction. Denser populations inland will lead to more runoff and siltation. Effects of human perturbations can be explored with metapopulation theory since they translate to increases in patch-mortality and decreases in patch-colonization (=regeneration). All such changes will result in a habitat with overall fewer settled patches, so fewer live reefs. If rescue effects are included, bifurcations in system dynamics will allow for many empty patches and, depending on system state relative to stable and unstable equilibria, a part-empty system may either trend towards stability at higher patch occupancy or extinction. Thus, unless the disturbance history is known, it may be difficult to assess the direction of system trajectory-making management difficult. If habitat is decreased by destruction, rescue effects become even more important as extinction-debt, accumulated by efficient competitors with weaker dispersal ability, is realized. Easily visible trends in human population dynamics combined with well-established and tested ecological theory give a clear, intuitive, yet quantifiable guide to the severity of survival challenges faced by coral reefs. Management challenges and required actions can be clearly shown and, contrary to frequent claims, no scientific ambiguity exists with regards to the serious threat posed to coral reefs by humankind's continued numerical increase.

A revised Holocene coral sea-level database from the Florida reef tract, USA.

The coral reefs and mangrove habitats of the south Florida region have long been used in sea-level studies for the western Atlantic because of their broad geographic extent and composition of sea-level tracking biota. The data from this region have been used to support several very different Holocene sea-level reconstructions (SLRs) over the years. However, many of these SLRs did not incorporate all available coral-based data, in part because detailed characterizations necessary for inclusion into sea-level databases were lacking. Here, we present an updated database comprised of 303 coral samples from published sources that we extensively characterized for the first time. The data were carefully screened by evaluating and ranking the visual taphonomic characteristics of every dated sample within the database, which resulted in the identification of 134 high-quality coral samples for consideration as suitable sea-level indicators. We show that our database largely agrees with the most recent SLR for south Florida over the last ∼7,000 years; however, the early Holocene remains poorly characterized because there are few high-quality data spanning this period. Suggestions to refine future Holocene SLRs in the region are provided including filling spatial and temporal data gaps of coral samples, particularly from the early Holocene, as well as constructing a more robust peat database to better constrain sea-level variability during the middle to late Holocene. Our database and taphonomic-ranking protocol provide a framework for researchers to evaluate data-selection criteria depending on the robustness of their sea-level models.

Octocoral populations and connectivity in continental Ecuador and Galápagos, Eastern Pacific.

Octocorals are important zoobenthic organisms, contributing to structural heterogeneity and species diversity on hardgrounds. Their persistence amidst global coral reef degradation and ocean acidification, has prompted renewed interest in this taxon. Octocoral assemblages at 52 sites in continental Ecuador and Galápagos (23 species, 3742 colonies) were examined for composition, size distributions within and among populations, and connectivity patterns based on ocean current models. Species richness varied from 1 to 14 species per site, with the richest sites on the continent. Three assemblage clusters were recognised based on species richness and population size, one with a mix of sites from the mainland and Galápagos (defined by Muricea fruticosa and Leptogorgia alba, Muricea plantaginea and Pacifigorgia darwinii), the second from Santa Elena in southern Ecuador (defined by M. plantaginea and L. alba) and the third from the northernmost sites on the continent, in Esmeraldas (defined by Muricea fruticosa, Heterogorgia hickmani, Leptogorgia manabiensis). Based on biophysical larval flow models with 30, 60, 90-day Pelagic Larval Duration, good connectivity existed along the South American mainland, and from the continent to Galápagos. Connectivity between Galápagos, Cocos, Malpelo and the Colombian mainland may explain the wide distribution of L. alba. Muricea plantaginea had the densest populations with the largest colonies and therewith was an important habitat provider both in continental Ecuador and Galápagos. Continental Ecuador harbours the most speciose populations of octocorals so far recorded in the southern Eastern Tropical Pacific (ETP). Most species were uncommon and possibly vulnerable to local extirpation. The present study may serve as a base line to determine local and regional impacts of future disturbances on ETP octocorals.

Biophysical model of coral population connectivity in the Arabian/Persian Gulf.

The coral reef ecosystems of the Arabian/Persian Gulf (the Gulf) are facing profound pressure from climate change (extreme temperatures) and anthropogenic (land-use and population-related) stressors. Increasing degradation at local and regional scales has already resulted in widespread coral cover reduction. Connectivity, the transport and exchange of larvae among geographically separated populations, plays an essential role in recovery and maintenance of biodiversity and resilience of coral reef populations. Here, an oceanographic model in 3-D high-resolution was used to simulate particle dispersion of "virtual larvae." We investigated the potential physical connectivity of coral reefs among different regions in the Gulf. Simulations reveal that basin-scale circulation is responsible for broader spatial dispersion of the larvae in the central region of the Gulf, and tidally-driven currents characterized the more localized connectivity pattern in regions along the shores in the Gulf's southern part. Results suggest predominant self-recruitment of reefs with highest source and sink ratios along the Bahrain and western Qatar coasts, followed by the south eastern Qatar and continental Abu Dhabi coast. The central sector of the Gulf is suggested as recruitment source in a stepping-stone dynamics. Recruitment intensity declined moving away from the Straits of Hormuz. Connectivity varied in models assuming passive versus active mode of larvae movement. This suggests that larval behaviour needs to be taken into consideration when establishing dispersion models, and establishing conservation strategies for these vulnerable ecosystems.

A tropical eastern Pacific invasive brittle star species (Echinodermata: Ophiuroidea) reaches southeastern Florida.

The invasive brittle star Ophiothela mirabilis (family Ophiotrichidae), a tropical Indo-Pacific endemic species, first reported in Atlantic waters off southern Brazil in 2000, has extended its range northward to the Caribbean Sea, to the Lesser Antilles in 2011, and was first reported in south Florida in January 2019. Its occurrence in southeast Florida extends along nearly 70km of coastline, from near the Port of Miami, Miami-Dade County, northward to Deerfield Beach, Broward County. It occurs abundantly as an epizoite on octocorals, attaining population densities of 25 individuals and more per 10-cm long octocoral stem. The surface texture of octocoral hosts (rough, smooth) did not affect the densities of the ophiuroid epizoites, and there were significantly greater abundances on octocorals during two winter sampling periods than in the summer. Beige and orange-coloured morphs are sometimes present on the same octocoral stem. Gut content analysis supported a suspension feeding mode, revealing essentially identical ingested items in both colour morphs with a preponderance of amorphous detritus and filamentous algae. Molecular genetic evidence (COI & 16s) has established the identity of O. mirabilis and its relationship to invasive Brazilian populations. The orange and beige morphs form two distinct, but closely related lineages that may represent two separate introductions. The orange morph shares haplotypes with Brazilian and Caribbean specimens suggesting a further range expansion of the 'original' invasion. The beige morph, however, shares haplotypes with specimens from the Mexican Pacific and Peru and potentially represents a secondary introduction. Traits promoting dispersal and establishment of this species in new habitats are manifold: vagility and ability to cling tightly to diverse host taxa (e.g. sponges, cnidarians, bryozoans, and echinoderms), frequent asexual reproduction (fissiparity), suspension feeding, including a wide range of dietary items, possession of integument-covered ossicles and arm spines offering protection from predators, and an effective competitive edge over associated microbiota for substrate space.

Measured and predicted acute toxicity of phenanthrene and MC252 crude oil to vertically migrating deep-sea crustaceans.

Deep-water column micronekton play a key role in oceanic food webs and represent an important trophic link between deep- and shallow-water ecosystems. Thus, the potential impacts of sub-surface hydrocarbon plumes on these organisms are critical to developing a more complete understanding of ocean-wide effects resulting from deep-sea oil spills. This work was designed to advance the understanding of hydrocarbon toxicity in several ecologically important deep-sea micronekton species using controlled laboratory exposures aimed at determining lethal threshold exposure levels. The current study confirmed the results previously determined for five deep-sea micronekton by measuring lethal threshold levels for phenanthrene between 81.2 and 277.5 µg/L. These results were used to calibrate the target lipid model and to calculate a critical target lipid body burden for each species. In addition, an oil solubility model was used to predict the acute toxicity of MC252 crude oil to vertically migrating crustaceans, Janicella spinacauda and Euphausiidae spp., and to compare the predictions with results of a 48-h constant exposure toxicity test with passive-dosing. Results confirmed that the tested deep-sea micronekton appear more sensitive than many other organisms when exposed to dissolved oil, but baseline stress complicated interpretation of results.

Short-term toxicity of 1-methylnaphthalene to Americamysis bahia and 5 deep-sea crustaceans.

There are few studies that have evaluated hydrocarbon toxicity to vertically migrating deep-sea micronekton. Crustaceans were collected alive using a 9-m2 Tucker trawl with a thermally insulated cod end and returned to the laboratory in 10 °C seawater. Toxicity of the polycyclic aromatic hydrocarbon 1-methylnaphthalene to Americamysis bahia, Janicella spinacauda, Systellaspis debilis, Sergestes sp., Sergia sp., and a euphausiid species was assessed in a constant exposure toxicity test utilizing a novel passive dosing toxicity testing protocol. The endpoint of the median lethal concentration tests was mortality, and the results revealed high sensitivity of the deep-sea micronekton compared with other species for which these data are available. Threshold concentrations were also used to calculate critical target lipid body burdens using the target lipid model. Environ Toxicol Chem 2017;36:3415-3423. © 2017 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals, Inc. on behalf of SETAC.

Acute and subacute toxicity of the polycyclic aromatic hydrocarbon 1-methylnaphthalene to the shallow-water coral Porites divaricata: Application of a novel exposure protocol.

Previous research evaluating hydrocarbon toxicity to corals and coral reefs has generally focused on community-level effects, and results often are not comparable between studies because of variability in hydrocarbon exposure characterization and evaluation of coral health and mortality during exposure. Toxicity of the polycyclic aromatic hydrocarbon 1-methylnaphthalene to the coral Porites divaricata was assessed in a constant exposure toxicity test utilizing a novel toxicity testing protocol uniquely applicable to shallow-water corals, which considered multiple assessment metrics and evaluated the potential for post-exposure mortality and/or recovery. Acute and subacute effects (gross morphological changes, photosynthetic efficiency, mortality, and histologic cellular changes) were evaluated during pre-exposure (4 wk), exposure (48 h), and post-exposure recovery (4 wk) periods. Coral condition scores were used to determine a 48-h median effective concentration of 7442 µg/L. Significant physical and histological changes resulted from exposure to 640 µg/L and 5427 µg/L 1-methylnaphthalene, with a 1-d to 3-d delay in photosynthetic efficiency effects (ΔF/Fm). Pigmented granular amoebocyte area was found to be a potentially useful sublethal endpoint for this species. Coral mortality was used to estimate a 48-h median lethal concentration of 12 123 µg/L. Environ Toxicol Chem 2017;36:212-219. © 2016 SETAC.

Thermal tolerances of reef corals in the Gulf: a review of the potential for increasing coral survival and adaptation to climate change through assisted translocation.

Corals in the Gulf withstand summer temperatures up to 10 °C higher than corals elsewhere and have recovered from extreme temperature events in 10 years or less. This heat-tolerance of Gulf corals has positive implications for the world's coral populations to adapt to increasing water temperatures. However, survival of Gulf corals has been severely tested by 35-37 °C temperatures five times in the last 15 years, each time causing extensive coral bleaching and mortality. Anticipated future temperature increases may therefore challenge survival of already highly stressed Gulf corals. Previously proposed translocation of Gulf corals to introduce temperature-adapted corals outside of the Gulf is assessed and determined to be problematical, and to be considered a tool of last resort. Coral culture and transplantation within the Gulf is feasible for helping maintain coral species populations and preserving genomes and adaptive capacities of Gulf corals that are endangered by future thermal stress events.

Functional composition of Chaetodon butterflyfishes at a peripheral and extreme coral reef location, the Persian Gulf.

The functional composition of reef fish assemblages is highly conserved across large biogeographic areas, but it is unknown whether assembly rules hold at biogeographical and environmental extremes for coral reefs. This study examined the functional composition of butterflyfishes in the Persian Gulf, Musandam Peninsula, and Gulf of Oman. Only five species of butterflyfishes were recorded during this study, and mostly just in the Gulf of Oman. Unlike most locations in the Indo-Pacific where butterflyfish assemblages are dominated by obligate corallivores, the only obligate corallivore recorded, Chaetodon melapterus, was rare or absent at all locations. The most common and widespread species was Chaetodon nigropunctatus, which is shown to be a facultative corallivore. The diversity of butterflyfishes in the Persian Gulf is likely to have been constrained by its' biogeographical history and isolation, but functional composition appears to be further affected by limited abundance of prey corals and harsh environmental conditions.

Human impact on atolls leads to coral loss and community homogenisation: a modeling study.

We explore impacts on pristine atolls subjected to anthropogenic near-field (human habitation) and far-field (climate and environmental change) pressure. Using literature data of human impacts on reefs, we parameterize forecast models to evaluate trajectories in coral cover under impact scenarios that primarily act via recruitment and increased mortality of larger corals. From surveys across the Chagos, we investigate the regeneration dynamics of coral populations distant from human habitation after natural disturbances. Using a size-based mathematical model based on a time-series of coral community and population data from 1999-2006, we provide hind- and forecast data for coral population dynamics within lagoons and on ocean-facing reefs verified against monitoring from 1979-2009. Environmental data (currents, temperatures) were used for calibration. The coral community was simplified into growth typologies: branching and encrusting, arboresent and massive corals. Community patterns observed in the field were influenced by bleaching-related mortality, most notably in 1998. Survival had been highest in deep lagoonal settings, which suggests a refuge. Recruitment levels were higher in lagoons than on ocean-facing reefs. When adding stress by direct human pressure, climate and environmental change as increased disturbance frequency and modified recruitment and mortality levels (due to eutrophication, overfishing, pollution, heat, acidification, etc), models suggest steep declines in coral populations and loss of community diversification among habitats. We found it likely that degradation of lagoonal coral populations would impact regeneration potential of all coral populations, also on ocean-facing reefs, thus decreasing reef resilience on the entire atoll.

Red Sea coral reef trajectories over 2 decades suggest increasing community homogenization and decline in coral size.

Three independent line intercept transect surveys on northern Red Sea reef slopes conducted in 1988/9 and 1997/8 in Egypt and from 2006-9 in Saudi Arabia were used to compare community patterns and coral size. Coral communities showed scale-dependent variability, highest at fine spatial and taxonomic scale (species-specific within and among reef patterns). At coarser scale (generic pattern across regions), patterns were more uniform (regionally consistent generic dominance on differently exposed reef slopes and at different depths). Neither fine- nor coarse-scale patterns aligned along the sampled 1700 km latitudinal gradient. Thus, a latitudinal gradient that had been described earlier from comparable datasets, separating the Red Sea into three faunistic zones, was no longer apparent. This may indicate subtle changes in species distributions. Coral size, measured as corrected average intercept of corals in transects, had decreased from 1997 to 2009, after having remained constant from 1988 to 1997. Recruitment had remained stable (∼12 juvenile corals per m(2)). Size distributions had not changed significantly but large corals had declined over 20 years. Thus, data from a wide range of sites taken over two decades support claims by others that climate change is indeed beginning to show clear effects on Red Sea reefs.

Present limits to heat-adaptability in corals and population-level responses to climate extremes.

Climate change scenarios suggest an increase in tropical ocean temperature by 1-3°C by 2099, potentially killing many coral reefs. But Arabian/Persian Gulf corals already exist in this future thermal environment predicted for most tropical reefs and survived severe bleaching in 2010, one of the hottest years on record. Exposure to 33-35°C was on average twice as long as in non-bleaching years. Gulf corals bleached after exposure to temperatures above 34°C for a total of 8 weeks of which 3 weeks were above 35°C. This is more heat than any other corals can survive, providing an insight into the present limits of holobiont adaptation. We show that average temperatures as well as heat-waves in the Gulf have been increasing, that coral population levels will fluctuate strongly, and reef-building capability will be compromised. This, in combination with ocean acidification and significant local threats posed by rampant coastal development puts even these most heat-adapted corals at risk. WWF considers the Gulf ecoregion as "critically endangered". We argue here that Gulf corals should be considered for assisted migration to the tropical Indo-Pacific. This would have the double benefit of avoiding local extinction of the world's most heat-adapted holobionts while at the same time introducing their genetic information to populations naïve to such extremes, potentially assisting their survival. Thus, the heat-adaptation acquired by Gulf corals over 6 k, could benefit tropical Indo-Pacific corals who have <100 y until they will experience a similarly harsh climate. Population models suggest that the heat-adapted corals could become dominant on tropical reefs within ∼20 years.