Distinct fine-scale variations in calcification control revealed by high-resolution 2D boron laser images in the cold-water coral Lophelia pertusa

Coral calcification is a complex biologically controlled process of hard skeleton formation, and it is influenced by environmental conditions. The chemical composition of coral skeletons responds to calcification conditions and can be used to gain insights into both the control asserted by the organism and the environment. Boron and its isotopic composition have been of particular interest because of links to carbon chemistry and pH. In this study, we acquired high-resolution boron images (concentration and isotopes) in a skeleton sample of the azooxanthellate cold-water coral Lophelia pertusa. We observed high boron variability at a small spatial scale related to skeletal structure. This implies differences in calcification control during different stages of skeleton formation. Our data point to bicarbonate active transport as a critical pathway during early skeletal growth, and the variable activity rates explain the majority of the observed boron systematic

Discrete Pulses of Cooler Deep Water Can Decelerate Coral Bleaching During Thermal Stress: Implications for Artificial Upwelling During Heat Stress Events

Global warming is considered to be the most severe threat to coral reefs globally, which makes it important for scientists to develop novel strategies that mitigate the impact of warming on corals and associated habitats. Artificial upwelling of cooler deep water to the surface layer may be a possible mitigation/management tool. In this study, we investigated the effect of simulated artificial upwelling with deep water off Bermuda collected at 50 m (24°C) and 100 m (20°C) on coral symbiont biology of 3 coral species (Montastrea cavernosa, Porites astreoides, and Pseudodiploria strigosa) in a temperature stress experiment. The following treatments were applied over a period of 3 weeks: (i) control at 28°C (ii) heat at 31°C, (iii) heat at 31°C+ deep water from 50 m depth, and (iv) heat at 31°C+ deep water from 100 m depth. Artificial upwelling was simulated over a period of 25 min on a daily basis resulting in a reduction of temperature for 2 h per day and the following degree-heating-weeks: 5.7°C-weeks for ii, 4.6°C-weeks for iii and 4.2°C-weeks for iv. Comparative analysis of photosynthetic rate, chlorophyll-a concentration and zooxanthellae density revealed a reduction of heat stress responses in artificial upwelling treatments in 2 of the 3 investigated species, and a stronger positive effect of 100-m water than 50-m water. These results indicate that artificial upwelling could be an effective strategy to mitigate coral bleaching during heat stress events allowing corals to adjust to increasing temperatures more gradually. It will still be necessary to further explore the ecological benefits as well as potential ecosystem impacts associated with different artificial upwelling scenarios to carefully implement an effective in situ artificial upwelling strategy in coral reefs

Modeling coral bleaching mitigation potential of water vertical translocation – an analogue to geoengineered artificial upwelling

Artificial upwelling (AU) is a novel geoengineering technology that brings seawater from the deep ocean to the surface. Within the context of global warming, AU techniques are proposed to reduce sea surface temperature at times of thermal stress around coral reefs. A computationally fast but coarse 3D Earth System model (3.6° longitude × 1.8° latitude) was used to investigate the environmental impacts of hypothetically implemented AU strategies in the Great Barrier Reef, South China Sea, and Hawaiian regions. While omitting the discussion on sub-grid hydrology, we simulated in our model a water translocation from either 130 or 550 m depth to sea surface at rates of 1 or 50 m3 s−1 as analogues to AU implementation. Under the Representative Concentration Pathway 8.5 emissions scenario from year 2020 on, the model predicted a prevention of coral bleaching until the year 2099 when AU was implemented, except under the least intense AU scenario (water from 130 m depth at 1 m3 s−1). Yet, intense AU implementation (water from 550 m depth at 50 m3 s-1) will likely have adverse effects on coral reefs by overcooling the surface water, altering salinity, decreasing calcium carbonate saturation, and considerably increasing nutrient levels. Our result suggests that if we utilize AU for mitigating coral bleaching during heat stress, AU implementation needs to be carefully designed with respect to AU’s location, depth, intensity and duration so that undesirable environmental effects are minimized. Following a proper installation and management procedure, however, AU has the potential to decelerate destructive bleaching events and buy corals more time to adjust to climate change

Large-amplitude internal waves sustain coral health during thermal stress

Ocean warming is a major threat for coral reefs causing widespread coral bleaching and mortality. Potential refugia are thus crucial for coral survival. Exposure to large-amplitude internal waves (LAIW) mitigated heat stress and ensured coral survival and recovery during and after an extreme heat anomaly. The physiological status of two common corals, Porites lutea and Pocillopora meandrina, was monitored in host and symbiont traits, in response to LAIW-exposure throughout the unprecedented 2010 heat anomaly in the Andaman Sea. LAIW-exposed corals of both species survived and recovered, while LAIW-sheltered corals suffered partial and total mortality in P. lutea and P. meandrina, respectively. LAIW are ubiquitous in the tropics and potentially generate coral refuge areas. As thermal stress to corals is expected to increase in a warming ocean, the mechanisms linking coral bleaching to ocean dynamics will be crucial to predict coral survival on a warming plane

Towards enhancing coral heat tolerance: a “microbiome transplantation” treatment using inoculations of homogenized coral tissues

Background: Microbiome manipulation could enhance heat tolerance and help corals survive the pressures of ocean warming. We conducted coral microbiome transplantation (CMT) experiments using the reef-building corals, Pocillopora and Porites, and investigated whether this technique can benefit coral heat resistance while modifying the bacterial microbiome. Initially, heat-tolerant donors were identified in the wild. We then used fresh homogenates made from coral donor tissues to inoculate conspecific, heat-susceptible recipients and documented their bleaching responses and microbiomes by 16S rRNA gene metabarcoding. Results: Recipients of both coral species bleached at lower rates compared to the control group when exposed to short-term heat stress (34 °C). One hundred twelve (Pocillopora sp.) and sixteen (Porites sp.) donor-specific bacterial species were identified in the microbiomes of recipients indicating transmission of bacteria. The amplicon sequence variants of the majority of these transmitted bacteria belonged to known, putatively symbiotic bacterial taxa of corals and were linked to the observed beneficial effect on the coral stress response. Microbiome dynamics in our experiments support the notion that microbiome community evenness and dominance of one or few bacterial species, rather than host-species identity, were drivers for microbiome stability in a holobiont context. Conclusions: Our results suggest that coral recipients likely favor the uptake of putative bacterial symbionts, recommending to include these taxonomic groups in future coral probiotics screening efforts. Our study suggests a scenario where these donor-specific bacterial symbionts might have been more efficient in supporting the recipients to resist heat stress compared to the native symbionts present in the control group. These findings urgently call for further experimental investigation of the mechanisms of action underlying the beneficial effect of CMT and for field-based long-term studies testing the persistence of the effect. [MediaObject not available: see fulltext.]

Using B isotopes and B/Ca in corals from low saturation springs to constrain calcification mechanisms

Ocean acidification is expected to negatively impact calcifying organisms, yet we lack understanding of their acclimation potential in the natural environment. Here we measured geochemical proxies (δ11B and B/Ca) in Porites astreoides corals that have been growing for their entire life under low aragonite saturation (Ωsw: 0.77–1.85). This allowed us to assess the ability of these corals to manipulate the chemical conditions at the site of calcification (Ωcf), and hence their potential to acclimate to changing Ωsw. We show that lifelong exposure to low Ωsw did not enable the corals to acclimate and reach similar Ωcf as corals grown under ambient conditions. The lower Ωcf at the site of calcification can explain a large proportion of the decreasing P. astreoides calcification rates at low Ωsw. The naturally elevated seawater dissolved inorganic carbon concentration at this study site shed light on how different carbonate chemistry parameters affect calcification conditions in corals

Role of hydrodynamics in shaping chemical habitats and modulating the responses of coastal benthic systems to ocean global change

Marine coastal zones are highly productive, and dominated by engineer species (e.g. macrophytes, molluscs, corals) that modify the chemistry of their surrounding seawater via their metabolism, causing substantial fluctuations in oxygen, dissolved inorganic carbon, pH, and nutrients. The magnitude of these biologically driven chemical fluctuations is regulated by hydrodynamics, can exceed values predicted for the future open ocean, and creates chemical patchiness in subtidal areas at various spatial (µm to meters) and temporal (minutes to months) scales. Although the role of hydrodynamics is well explored for planktonic communities, its influence as a crucial driver of benthic organism and community functioning is poorly addressed, particularly in the context of ocean global change. Hydrodynamics can directly modulate organismal physiological activity or indirectly influence an organism's performance by modifying its habitat. This review addresses recent developments in (i) the influence of hydrodynamics on the biological activity of engineer species, (ii) the description of chemical habitats resulting from the interaction between hydrodynamics and biological activity, (iii) the role of these chemical habitat as refugia against ocean acidification and deoxygenation, and (iv) how species living in such chemical habitats may respond to ocean global change. Recommendations are provided to integrate the effect of hydrodynamics and environmental fluctuations in future research, to better predict the responses of coastal benthic ecosystems to ongoing ocean global change

Large-amplitude internal waves benefit corals during thermal stress

Tropical scleractinian corals are particularly vulnerable to global warming as elevated sea surface temperatures (SSTs) disrupt the delicate balance between the coral host and their algal endosymbionts, leading to symbiont expulsion, mass bleaching and mortality. While satellite sensing of SST has proved a reliable predictor of coral bleaching at the regional scale, there are large deviations in bleaching severity and mortality on the local scale that are poorly understood. Here, we show that internal waves play a major role in explaining local coral bleaching and mortality patterns in the Andaman Sea. Despite a severe region-wide SST anomaly in May 2010, frequent upslope intrusions of cold sub-pycnocline waters due to breaking large-amplitude internal waves (LAIW) mitigated coral bleaching and mortality in shallow waters. In LAIW-sheltered waters, by contrast, bleaching-susceptible species suffered severe bleaching and total mortality. These findings suggest that LAIW benefit coral reefs during thermal stress and provide local refugia for bleaching-susceptible corals. LAIW are ubiquitous in tropical stratified waters and their swash zones may thus be important conservation areas for the maintenance of coral diversity in a warming climate. Taking LAIW into account can significantly improve coral bleaching predictions and provide a valuable tool for coral reef conservation and management

The role of pH up-regulation in response to nutrient-enriched, low-pH groundwater discharge

Highlights • Dual geochemical approach using δ11B and B/Ca to evaluate coral calcifying fluids from West Maui, Hawai'i. • NMR analysis confirms boron is present as borate with no evidence of boric acid inclusion. • Increased pH up-regulation in corals exposed to high nutrient / low pH submarine groundwater discharge. • Calcifying fluid aragonite saturate state 9 to 10 times higher than ambient seawater. • Up-regulation as an internal coping mechanism to combat multiple stressors from land-based sources of pollution. Coral reefs and their ecosystems are threatened by both global stressors, including increasing sea-surface temperatures and ocean acidification (OA), and local stressors such as land-based sources of pollution that can magnify the effects of OA. Corals can physiologically control the chemistry of their internal calcifying fluids (CF) and can thereby regulate their calcification process. Specifically, increasing aragonite saturation state in the CF (ΩCF) may allow corals to calcify even under external low saturation conditions. Questions remain regarding the physiological processes that govern the CF chemistry and how they change in response to multiple stressors. To address this knowledge gap, the boron systematics (δ11B and B/Ca) were analyzed in tropical corals, Porites lobata, collected at submarine groundwater seeps impacted by the release of treated wastewater in west Maui, Hawai'i, to document the interactions between high nutrient / low pH seep water on CF carbonate chemistry. Results show substantial up-regulation of pH and dissolved inorganic carbon (DIC) with respect to seawater in P. lobata corals collected from within the wastewater impacted area at Kahekili Beach Park compared to the control site at Olowalu Beach. The ΩCF was 9 to 10 times higher than ambient seawater Ω, and 13 to 26% higher than in corals from the control site and from previously observed in tropical Porites spp. corals. Such elevated up-regulation suggests that corals exposed to nutrient-enriched, low pH effluent sustain CF supersaturated with respect to aragonite, possibly as an internal coping mechanism to combat multiple stressors from land-based sources of pollution. This elevated up-regulation has implications to coral vulnerability to future climate- and ocean-change scenarios

Calcification, skeletal structure and composition of the cold-water coral Desmophyllum dianthus

In the naturally acidified Comau Fjord (Chile), high densities of the cosmopolitan cold-water coral (CWC) Desmophyllum dianthus are found at or below aragonite saturation (Ωar ≤ 1). However, it is not known so far if seasonal changes in Ωar lead to seasonal differences in calcification rates and the corals’ ability to up-regulate the pH in the calcifying fluid (pHcf). In the present study, corals were sampled along both horizontal and vertical pH gradients (pHT = 7.6-7.9, Ωar = 0.76-1.45) in Comau Fjord. We compared D. dianthus’ calcification rates (buoyant weight technique) with the physico-chemical conditions in the water column (T, Ωar) in austral summer 2016/2017 and winter 2017. In order to determine the biological pHcf up-regulation of D. dianthus, the skeletal boron isotopic composition (δ11B) was measured in the upper part of the calyx between the septa, using a UV femtosecond laser ablation system connected to a multicollector inductively coupled plasma mass spectrometer (LA-MC-ICP-MS). Higher growth rates of D. dianthus were found in summer than in winter. Surprisingly, growth of D. dianthus was highest in undersaturated waters in both seasons (Ωar = 0.76 and 0.84) and cross-transplanted specimens were able to acclimatise to Ωar < 1. Therefore, the present study shows that Ωar alone is a poor predictor of D. dianthus growth. Skeletal analyses show a complex relationship between δ11B and the structure of the coral skeletons. δ11B measurements were highly variable, which may be attributed to the high calcification rates in the upper part of the coral calyx. Therefore, high resolution analyses of the skeletal composition and micro-structure will be conducted along the entire longitudinal section of D. dianthus skeletons using Raman microscopy and scanning electron microscopy (SEM). In addition, δ11B will be measured in different skeletal parts and compared to skeletal structure analyses for a reliable reconstruction of seawater pH at high temporal resolution using skeletons of D. dianthus grown under laboratory and field conditions (Comau Fjord, Chile)