Hidden heatwaves and severe coral bleaching linked to mesoscale eddies and thermocline dynamics.

The severity of marine heatwaves (MHWs) that are increasingly impacting ocean ecosystems, including vulnerable coral reefs, has primarily been assessed using remotely sensed sea-surface temperatures (SSTs), without information relevant to heating across ecosystem depths. Here, using a rare combination of SST, high-resolution in-situ temperatures, and sea level anomalies observed over 15 years near Moorea, French Polynesia, we document subsurface MHWs that have been paradoxical in comparison to SST metrics and associated with unexpected coral bleaching across depths. Variations in the depth range and severity of MHWs was driven by mesoscale (10s to 100s of km) eddies that altered sea levels and thermocline depths and decreased (2007, 2017 and 2019) or increased (2012, 2015, 2016) internal-wave cooling. Pronounced eddy-induced reductions in internal waves during early 2019 contributed to a prolonged subsurface MHW and unexpectedly severe coral bleaching, with subsequent mortality offsetting almost a decade of coral recovery. Variability in mesoscale eddy fields, and thus thermocline depths, is expected to increase with climate change, which, along with strengthening and deepening stratification, could increase the occurrence of subsurface MHWs over ecosystems historically insulated from surface ocean heating by the cooling effects of internal waves.

Response diversity in corals: hidden differences in bleaching mortality among cryptic Pocillopora species.

Variation among functionally similar species in their response to environmental stress buffers ecosystems from changing states. Functionally similar species may often be cryptic species representing evolutionarily distinct genetic lineages that are morphologically indistinguishable. However, the extent to which cryptic species differ in their response to stress, and could therefore provide a source of response diversity, remains unclear because they are often not identified or are assumed to be ecologically equivalent. Here, we uncover differences in the bleaching response between sympatric cryptic species of the common Indo-Pacific coral, Pocillopora. In April 2019, prolonged ocean heating occurred at Moorea, French Polynesia. 72% of pocilloporid colonies bleached after 22 d of severe heating (>8o C-days) at 10 m depth on the north shore fore reef. Colony mortality ranged from 11% to 42% around the island four months after heating subsided. The majority (86%) of pocilloporids that died from bleaching belonged to a single haplotype, despite twelve haplotypes, representing at least five species, being sampled. Mitochondrial (open reading frame) sequence variation was greater between the haplotypes that experienced mortality versus haplotypes that all survived than it was between nominal species that all survived. Colonies > 30 cm in diameter were identified as the haplotype experiencing the most mortality, and in 1125 colonies that were not genetically identified, bleaching and mortality increased with colony size. Mortality did not increase with colony size within the haplotype suffering the highest mortality, suggesting that size-dependent bleaching and mortality at the genus level was caused instead by differences among cryptic species. The relative abundance of haplotypes shifted between February and August, driven by declines in the same common haplotype for which mortality was estimated directly, at sites where heat accumulation was greatest, and where larger colony sizes occurred. The identification of morphologically indistinguishable species that differ in their response to thermal stress, but share a similar ecological function in terms of maintaining a coral-dominated state, has important consequences for uncovering response diversity that drives resilience, especially in systems with low or declining functional diversity.

High resolution spatiotemporal patterns of seawater temperatures across the Belize Mesoamerican Barrier Reef.

Coral reefs are under increasingly severe threat from climate change and other anthropogenic stressors. Anomalously high seawater temperatures in particular are known to cause coral bleaching (loss of algal symbionts in the family Symbiodiniaceae), which frequently leads to coral mortality. Remote sensing of sea surface temperature (SST) has served as an invaluable tool for monitoring physical conditions that can lead to bleaching events over relatively large scales (e.g. few kms to 100 s of kms). But, it is also well known that seawater temperatures within a site can vary significantly across depths due to the combined influence of solar heating of surface waters, water column thermal stratification, and cooling from internal waves and upwelling. We deployed small autonomous benthic temperature sensors at depths ranging from 0-40 m in fore reef, back reef, and lagoonal reef habitats on the Belize Mesoamerican Barrier Reef System from 2000-2019. These data can be used to calculate depth-specific climatologies across reef depths and sites, and emphasize the dynamic and spatially-variable nature of coral reef physical environments.

Spatial variations in the stable isotope composition of the benthic algae, Halimeda tuna, and implications for paleothermometry.

On Conch Reef, Florida Keys, USA we examined the effects of reef hydrography and topography on the patterns of stable isotope values (δ18O and δ13C) in the benthic green alga, Halimeda tuna. During the summer, benthic temperatures show high-frequency fluctuations (2 to 8 °C) associated with internal waves that advected cool, nutrient-rich water across the reef. The interaction between local water flow and reef morphology resulted in a highly heterogenous physical environment even within isobaths that likely influenced the growth regime of H. tuna. Variability in H. tuna isotopic values even among closely located individuals suggest biological responses to the observed environmental heterogeneity. Although isotopic composition of reef carbonate material can be used to reconstruct past temperatures (T(°C) = 14.2-3.6 (δ18OHalimeda - δ18Oseawater); r2 = 0.92), comparing the temperatures measured across the reef with that predicted by an isotopic thermometer suggests complex interactions between the environment and Halimeda carbonate formation at temporal and spatial scales not normally considered in mixed sediment samples. The divergence in estimated range between measured and predicted temperatures demonstrates the existence of species- and location-specific isotopic relationships with physical and environmental factors that should be considered in contemporary as well as ancient reef settings.

Upwelling buffers climate change impacts on coral reefs of the eastern tropical Pacific.

Corals of the eastern tropical Pacific live in a marginal and oceanographically dynamic environment. Along the Pacific coast of Panamá, stronger seasonal upwelling in the Gulf of Panamá in the east transitions to weaker upwelling in the Gulf of Chiriquí in the west, resulting in complex regional oceanographic conditions that drive differential coral-reef growth. Over millennial timescales, reefs in the Gulf of Chiriquí recovered more quickly from climatic disturbances compared with reefs in the Gulf of Panamá. In recent decades, corals in the Gulf of Chiriquí have also had higher growth rates than in the Gulf of Panamá. As the ocean continues to warm, however, conditions could shift to favor the growth of corals in the Gulf of Panamá, where upwelling may confer protection from high-temperature anomalies. Here we describe the recent spatial and temporal variability in surface oceanography of nearshore environments in Pacific Panamá and compare those conditions with the dynamics of contemporary coral-reef communities during and after the 2016 coral-bleaching event. Although both gulfs have warmed significantly over the last 150 yr, the annual thermal maximum in the Gulf of Chiriquí is increasing faster, and ocean temperatures there are becoming more variable than in the recent past. In contrast to historical trends, we found that coral cover, coral survival, and coral growth rates were all significantly higher in the Gulf of Panamá. Corals bleached extensively in the Gulf of Chiriquí following the 2015-2016 El Niño event, whereas upwelling in the Gulf of Panamá moderated the high temperatures caused by El Niño, allowing the corals largely to escape thermal stress. As the climate continues to warm, upwelling zones may offer a temporary and localized refuge from the thermal impacts of climate change, while reef growth in the rest of the eastern tropical Pacific continues to decline.

Fluctuating thermal environments of shallow-water rocky reefs in the Gulf of California, Mexico.

As part of a broad-scale study of the biogeography of rocky reefs in the Gulf of California, Mexico (GOC), we collected a continuous 1-yr temperature time series at ~5 m water depth at 16 sites spanning 5° of latitude and ~700 km along the western boundary of the basin. Throughout the region, thermal conditions were most variable in summer with fluctuations concentrated at diurnal and semi-diurnal frequencies, likely associated with solar and wind forcing and vertical water column oscillations forced by internal waves. Temperatures in winter were less variable than in summer, and minimum temperatures also differed among sites. Thermal variability integrated across the diurnal and semi-diurnal frequency bands was greatest near the Midriff Islands in the northern GOC and decreased toward the southern sites. Diurnal variability was greater than semi-diurnal variability at 13 of the 16 sites. A statistic-of-extremes analysis indicated shortest return times for cooling events in summer, and reef organisms at many of the sites may experience anomalous 2 to 5 °C cooling events multiple times per month. The significant extent of local temperature variability may play important roles in limiting species occurrences among sites across this biogeographic region.

Benthic responses to an Antarctic regime shift: food particle size and recruitment biology.

Polar ecosystems are bellwether indicators of climate change and offer insights into ecological resilience. In this study, we describe contrasting responses to an apparent regime shift of two very different benthic communities in McMurdo Sound, Antarctica. We compared species-specific patterns of benthic invertebrate abundance and size between the west (low productivity) and east (higher productivity) sides of McMurdo Sound across multiple decades (1960s-2010) to depths of 60 m. We present possible factors associated with the observed changes. A massive and unprecedented shift in sponge recruitment and growth on artificial substrata observed between the 1980s and 2010 contrasts with lack of dramatic sponge settlement and growth on natural substrata, emphasizing poorly understood sponge recruitment biology. We present observations of changes in populations of sponges, bryozoans, bivalves, and deposit-feeding invertebrates in the natural communities on both sides of the sound. Scientific data for Antarctic benthic ecosystems are scant, but we gather multiple lines of evidence to examine possible processes in regional-scale oceanography during the eight years in which the sea ice did not clear out of the southern portion of McMurdo Sound. We suggest that large icebergs blocked currents and advected plankton, allowed thicker multi-year ice, and reduced light to the benthos. This, in addition to a possible increase in iron released from rapidly melting glaciers, fundamentally shifted the quantity and quality of primary production in McMurdo Sound. A hypothesized shift from large to small food particles is consistent with increased recruitment and growth of sponges on artificial substrata, filter-feeding polychaetes, and some bryozoans, as well as reduced populations of bivalves and crinoids that favor large particles, and echinoderms Sterechinus neumayeri and Odontaster validus that predominantly feed on benthic diatoms and large phytoplankton mats that drape the seafloor after spring blooms. This response of different guilds of filter feeders to a hypothesized shift from large to small phytoplankton points to the enormous need for and potential value of holistic monitoring programs, particularly in pristine ecosystems, that could yield both fundamental ecological insights and knowledge that can be applied to critical conservation concerns as climate change continues.

Contribution of sea ice microbial production to Antarctic benthic communities is driven by sea ice dynamics and composition of functional guilds.

Organic matter produced by the sea ice microbial community (SIMCo) is an important link between sea ice dynamics and secondary production in near-shore food webs of Antarctica. Sea ice conditions in McMurdo Sound were quantified from time series of MODIS satellite images for Sept. 1 through Feb. 28 of 2007-2015. A predictable sea ice persistence gradient along the length of the Sound and evidence for a distinct change in sea ice dynamics in 2011 were observed. We used stable isotope analysis (δ13 C and δ15 N) of SIMCo, suspended particulate organic matter (SPOM) and shallow water (10-20 m) macroinvertebrates to reveal patterns in trophic structure of, and incorporation of organic matter from SIMCo into, benthic communities at eight sites distributed along the sea ice persistence gradient. Mass-balance analysis revealed distinct trophic architecture among communities and large fluxes of SIMCo into the near-shore food web, with the estimates ranging from 2 to 84% of organic matter derived from SIMCo for individual species. Analysis of patterns in density, and biomass of macroinvertebrate communities among sites allowed us to model net incorporation of organic matter from SIMCo, in terms of biomass per unit area (g/m2 ), into benthic communities. Here, organic matter derived from SIMCo supported 39 to 71 per cent of total biomass. Furthermore, for six species, we observed declines in contribution of SIMCo between years with persistent sea ice (2008-2009) and years with extensive sea ice breakout (2012-2015). Our data demonstrate the vital role of SIMCo in ecosystem function in Antarctica and strong linkages between sea ice dynamics and near-shore secondary productivity. These results have important implications for our understanding of how benthic communities will respond to changes in sea ice dynamics associated with climate change and highlight the important role of shallow water macroinvertebrate communities as sentinels of change for the Antarctic marine ecosystem.

Simulating social-ecological systems: the Island Digital Ecosystem Avatars (IDEA) consortium.

Systems biology promises to revolutionize medicine, yet human wellbeing is also inherently linked to healthy societies and environments (sustainability). The IDEA Consortium is a systems ecology open science initiative to conduct the basic scientific research needed to build use-oriented simulations (avatars) of entire social-ecological systems. Islands are the most scientifically tractable places for these studies and we begin with one of the best known: Moorea, French Polynesia. The Moorea IDEA will be a sustainability simulator modeling links and feedbacks between climate, environment, biodiversity, and human activities across a coupled marine-terrestrial landscape. As a model system, the resulting knowledge and tools will improve our ability to predict human and natural change on Moorea and elsewhere at scales relevant to management/conservation actions.

Influence of coral and algal exudates on microbially mediated reef metabolism.

Benthic primary producers in tropical reef ecosystems can alter biogeochemical cycling and microbial processes in the surrounding seawater. In order to quantify these influences, we measured rates of photosynthesis, respiration, and dissolved organic carbon (DOC) exudate release by the dominant benthic primary producers (calcifying and non-calcifying macroalgae, turf-algae and corals) on reefs of Mo'orea French Polynesia. Subsequently, we examined planktonic and benthic microbial community response to these dissolved exudates by measuring bacterial growth rates and oxygen and DOC fluxes in dark and daylight incubation experiments. All benthic primary producers exuded significant quantities of DOC (roughly 10% of their daily fixed carbon) into the surrounding water over a diurnal cycle. The microbial community responses were dependent upon the source of the exudates and whether the inoculum of microbes included planktonic or planktonic plus benthic communities. The planktonic and benthic microbial communities in the unamended control treatments exhibited opposing influences on DO concentration where respiration dominated in treatments comprised solely of plankton and autotrophy dominated in treatments with benthic plus plankon microbial communities. Coral exudates (and associated inorganic nutrients) caused a shift towards a net autotrophic microbial metabolism by increasing the net production of oxygen by the benthic and decreasing the net consumption of oxygen by the planktonic microbial community. In contrast, the addition of algal exudates decreased the net primary production by the benthic communities and increased the net consumption of oxygen by the planktonic microbial community thereby resulting in a shift towards net heterotrophic community metabolism. When scaled up to the reef habitat, exudate-induced effects on microbial respiration did not outweigh the high oxygen production rates of benthic algae, such that reef areas dominated with benthic primary producers were always estimated to be net autotrophic. However, estimates of microbial consumption of DOC at the reef scale surpassed the DOC exudation rates suggesting net consumption of DOC at the reef-scale. In situ mesocosm experiments using custom-made benthic chambers placed over different types of benthic communities exhibited identical trends to those found in incubation experiments. Here we provide the first comprehensive dataset examining direct primary producer-induced, and indirect microbially mediated alterations of elemental cycling in both benthic and planktonic reef environments over diurnal cycles. Our results highlight the variability of the influence of different benthic primary producers on microbial metabolism in reef ecosystems and the potential implications for energy transfer to higher trophic levels during shifts from coral to algal dominance on reefs.

Effects of coral reef benthic primary producers on dissolved organic carbon and microbial activity.

Benthic primary producers in marine ecosystems may significantly alter biogeochemical cycling and microbial processes in their surrounding environment. To examine these interactions, we studied dissolved organic matter release by dominant benthic taxa and subsequent microbial remineralization in the lagoonal reefs of Moorea, French Polynesia. Rates of photosynthesis, respiration, and dissolved organic carbon (DOC) release were assessed for several common benthic reef organisms from the backreef habitat. We assessed microbial community response to dissolved exudates of each benthic producer by measuring bacterioplankton growth, respiration, and DOC drawdown in two-day dark dilution culture incubations. Experiments were conducted for six benthic producers: three species of macroalgae (each representing a different algal phylum: Turbinaria ornata--Ochrophyta; Amansia rhodantha--Rhodophyta; Halimeda opuntia--Chlorophyta), a mixed assemblage of turf algae, a species of crustose coralline algae (Hydrolithon reinboldii) and a dominant hermatypic coral (Porites lobata). Our results show that all five types of algae, but not the coral, exuded significant amounts of labile DOC into their surrounding environment. In general, primary producers with the highest rates of photosynthesis released the most DOC and yielded the greatest bacterioplankton growth; turf algae produced nearly twice as much DOC per unit surface area than the other benthic producers (14.0±2.8 µmol h⁻¹ dm⁻²), stimulating rapid bacterioplankton growth (0.044±0.002 log10 cells h⁻¹) and concomitant oxygen drawdown (0.16±0.05 µmol L⁻¹ h⁻¹ dm⁻²). Our results demonstrate that benthic reef algae can release a significant fraction of their photosynthetically-fixed carbon as DOC, these release rates vary by species, and this DOC is available to and consumed by reef associated microbes. These data provide compelling evidence that benthic primary producers differentially influence reef microbial dynamics and biogeochemical parameters (i.e., DOC and oxygen availability, bacterial abundance and metabolism) in coral reef communities.

Marine reserve design: optimal size, habitats, species affinities, diversity, and ocean microclimate.

The design of marine reserves is complex and fraught with uncertainty. However, protection of critical habitat is of paramount importance for reserve design. We present a case study as an example of a reserve design based on fine-scale habitats, the affinities of exploited species to these habitats, adult mobility, and the physical forcing affecting the dynamics of the habitats. These factors and their interaction are integrated in an algorithm that determines the optimal size and location of a marine reserve for a set of 20 exploited species within five different habitats inside a large kelp forest in southern California. The result is a reserve that encompasses approximately 42% of the kelp forest. Our approach differs fundamentally from many other marine reserve siting methods in which goals of area, diversity, or biomass are targeted a priori. Rather, our method was developed to determine how large a reserve must be within a specific area to protect a self-sustaining assemblage of exploited species. The algorithm is applicable across different ecosystems, spatial scales, and for any number of species. The result is a reserve in which habitat value is optimized for a predetermined set of exploited species against the area left open to exploitation. The importance of fine-scale habitat definitions for the exploited species off La Jolla is exemplified by the spatial pattern of habitats and the stability of these habitats within the kelp forest, both of which appear to be determined by ocean microclimate.