Cold-water coral energy reserves and calcification in contrasting fjord environments.

The relationship between energy reserves of cold-water corals (CWCs) and their physiological performance remains largely unknown. In addition, it is poorly understood how the energy allocation to different metabolic processes might change with projected decreasing food supply to the deep sea in the future. This study explores the temporal and spatial variations of total energy reserves (proteins, carbohydrates and lipids) of the CWC Desmophyllum dianthus and their correlation with its calcification rate. We took advantage of distinct horizontal and vertical physico-chemical gradients in Comau Fjord (Chile) and examined the changes in energy reserves over one year in an in situ reciprocal transplantation experiment (20 m vs. 300 m and fjord head vs. mouth). Total energy reserves correlated positively with calcification rates. The fast-growing deep corals had higher and less variable energy reserves, while the slower-growing shallow corals showed pronounced seasonal changes in energy reserves. Novel deep corals (transplanted from shallow) were able to quickly increase both their calcification rates and energy reserves to similar levels as native deep corals. Our study shows the importance of energy reserves in sustaining CWC growth in spite of aragonite undersaturated conditions (deep corals) in the present, and potentially also future ocean.

Heterotrophy in marine animal forests in an era of climate change.

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scalable interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly, few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold-water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

Ecophysiological and behavioural response of juveniles of the Chilean cold-water coral Caryophyllia (Caryophyllia) huinayensis to increasing sediment loads.

Chilean Patagonia is a hotspot of biodiversity, harbouring cold-water corals (CWCs) that populate steep walls and overhangs of fjords and channels. Through anthropogenic activities such as deforestation, roadworks, aquafarming and increased landslide frequency, sediment input increases in the fjord region. While the absence of CWCs on moderately steep slopes has been suggested to reflect high vulnerability to sedimentation, experimental evidence has been lacking. Here, we investigated the sensitivity of CWCs to sediment stress, using juvenile Caryophyllia (Caryophyllia) huinayensis as a model. A 12-week aquarium experiment was conducted with three sediment loads: the average natural sediment concentration in Comau Fjord, 100- and 1000-fold higher sediment levels, expected from gravel road use and coastal erosion. Changes in coral mass and calyx dimensions, polyp expansion, tissue retraction and respiration were measured. For CWCs exposed to two and three order of magnitude higher sediment concentrations, 32% and 80% of the animals experienced a decrease in tissue cover, respectively, along with a decrease in respiration rate of 34% and 66%. Under the highest concentration corals showed reduced polyp expansion and a significantly reduced growth of ~ 95% compared to corals at natural concentration. The results show that C. huinayensis is affected by high sediment loads. As human activities that increase sedimentation steadily intensify, coastal planners need to consider detrimental effects on CWCs.

Ontogenetic differences in the response of the cold-water coral Caryophyllia huinayensis to ocean acidification, warming and food availability.

Cold-water corals (CWCs) are considered vulnerable to environmental changes. However, previous studies have focused on adult CWCs and mainly investigated the short-term effects of single stressors. So far, the effects of environmental changes on different CWC life stages are unknown, both for single and multiple stressors and over long time periods. Therefore, we conducted a six-month aquarium experiment with three life stages of Caryophyllia huinayensis to study their physiological response (survival, somatic growth, calcification and respiration) to the interactive effects of aragonite saturation (0.8 and 2.5), temperature (11 and 15 °C) and food availability (8 and 87 µg C L-1). The response clearly differed between life stages and measured traits. Elevated temperature and reduced feeding had the greatest effects, pushing the corals to their physiological limits. Highest mortality was observed in adult corals, while calcification rates decreased the most in juveniles. We observed a three-month delay in response, presumably because energy reserves declined, suggesting that short-term experiments overestimate coral resilience. Elevated summer temperatures and reduced food supply are likely to have the greatest impact on live CWCs in the future, leading to reduced coral growth and population shifts due to delayed juvenile maturation and high adult mortality.

Life cycle of the cold-water coral Caryophyllia huinayensis.

Little is known about the biology of cold-water corals (CWCs), let alone the reproduction and early life stages of these important deep-sea foundation species. Through a three-year aquarium experiment, we described the reproductive mode, larval release periodicity, planktonic stage, larval histology, metamorphosis and post-larval development of the solitary scleractinian CWC Caryophyllia (Caryophyllia) huinayensis collected in Comau Fjord, Chilean Patagonia. We found that C. huinayensis is a brooder releasing 78.4 ± 65.9 (mean ± standard deviation [SD]) planula larvae throughout the year, a possible adaptation to low seasonality. Planulae had a length of 905 ± 114 µm and showed a well-developed gastrovascular system. After 8 ± 9.3 days (d), the larvae settled, underwent metamorphosis and developed the first set of tentacles after 2 ± 1.5 d. Skeletogenesis, zooplankton feeding and initiation of the fourth set of tentacles started 5 ± 2.1 d later, 21 ± 12.9 d, and 895 ± 45.9 d after settlement, respectively. Our study shows that the ontogenetic timing of C. huinayensis is comparable to that of some tropical corals, despite lacking zooxanthellae.

Ciliary flows in corals ventilate target areas of high photosynthetic oxygen production.

Most tropical corals live in symbiosis with Symbiodiniaceae algae whose photosynthetic production of oxygen (O2) may lead to excess O2 in the diffusive boundary layer (DBL) above the coral surface. When flow is low, cilia-induced mixing of the coral DBL is vital to remove excess O2 and prevent oxidative stress that may lead to coral bleaching and mortality. Here, we combined particle image velocimetry using O2-sensitive nanoparticles (sensPIV) with chlorophyll (Chla)-sensitive hyperspectral imaging to visualize the microscale distribution and dynamics of ciliary flows and O2 in the coral DBL in relation to the distribution of Symbiodiniaceae Chla in the tissue of the reef building coral, Porites lutea. Curiously, we found an inverse relation between O2 in the DBL and Chla in the underlying tissue, with patches of high O2 in the DBL above low Chla in the underlying tissue surrounding the polyp mouth areas and pockets of low O2 concentrations in the DBL above high Chla in the coenosarc tissue connecting neighboring polyps. The spatial segregation of Chla and O2 is related to ciliary-induced flows, causing a lateral redistribution of O2 in the DBL. In a 2D transport-reaction model of the coral DBL, we show that the enhanced O2 transport allocates parts of the O2 surplus to areas containing less chla, which minimizes oxidative stress. Cilary flows thus confer a spatially complex mass transfer in the coral DBL, which may play an important role in mitigating oxidative stress and bleaching in corals.

Environmental stability and phenotypic plasticity benefit the cold-water coral Desmophyllum dianthus in an acidified fjord.

The stratified Chilean Comau Fjord sustains a dense population of the cold-water coral (CWC) Desmophyllum dianthus in aragonite supersaturated shallow and aragonite undersaturated deep water. This provides a rare opportunity to evaluate CWC fitness trade-offs in response to physico-chemical drivers and their variability. Here, we combined year-long reciprocal transplantation experiments along natural oceanographic gradients with an in situ assessment of CWC fitness. Following transplantation, corals acclimated fast to the novel environment with no discernible difference between native and novel (i.e. cross-transplanted) corals, demonstrating high phenotypic plasticity. Surprisingly, corals exposed to lowest aragonite saturation (Ωarag < 1) and temperature (T < 12.0 °C), but stable environmental conditions, at the deep station grew fastest and expressed the fittest phenotype. We found an inverse relationship between CWC fitness and environmental variability and propose to consider the high frequency fluctuations of abiotic and biotic factors to better predict the future of CWCs in a changing ocean.

Seasonal and diel variations in the vertical distribution, composition, abundance and biomass of zooplankton in a deep Chilean Patagonian Fjord.

Comau Fjord is a stratified Chilean Patagonian Fjord characterized by a shallow brackish surface layer and a >400 m layer of aragonite-depleted subsurface waters. Despite the energetic burden of low aragonite saturation levels to calcification, Comau Fjord harbours dense populations of cold-water corals (CWC). While this paradox has been attributed to a rich supply of zooplankton, supporting abundance and biomass data are so far lacking. In this study, we investigated the seasonal and diel changes of the zooplankton community over the entire water column. We used a Nansen net (100 µm mesh) to take stratified vertical hauls between the surface and the bottom (0-50-100-200-300-400-450 m). Samples were scanned with a ZooScan, and abundance, biovolume and biomass were determined for 41 taxa identified on the web-based platform EcoTaxa 2.0. Zooplankton biomass was the highest in summer (209 g dry mass m-2) and the lowest in winter (61 g dry mass m-2). Abundance, however, peaked in spring, suggesting a close correspondence between reproduction and phytoplankton spring blooms (Chl a max. 50.86 mg m-3, 3 m depth). Overall, copepods were the most important group of the total zooplankton community, both in abundance (64-81%) and biovolume (20-70%) followed by mysids and chaetognaths (in terms of biovolume and biomass), and nauplii and Appendicularia (in terms of abundance). Throughout the year, diel changes in the vertical distribution of biomass were found with a daytime maximum in the 100-200 m depth layer and a nighttime maximum in surface waters (0-50 m), associated with the diel vertical migration of the calanoid copepod family Metridinidae. Diel differences in integrated zooplankton abundance, biovolume and biomass were probably due to a high zooplankton patchiness driven by biological processes (e.g., diel vertical migration or predation avoidance), and oceanographic processes (estuarine circulation, tidal mixing or water column stratification). Those factors are considered to be the main drivers of the zooplankton vertical distribution in Comau Fjord.

The carbon and nitrogen budget of Desmophyllum dianthus-a voracious cold-water coral thriving in an acidified Patagonian fjord.

In the North Patagonian fjord region, the cold-water coral (CWC) Desmophyllum dianthus occurs in high densities, in spite of low pH and aragonite saturation. If and how these conditions affect the energy demand of the corals is so far unknown. In a laboratory experiment, we investigated the carbon and nitrogen (C, N) budget of D. dianthus from Comau Fjord under three feeding scenarios: (1) live fjord zooplankton (100-2,300 µm), (2) live fjord zooplankton plus krill (>7 mm), and (3) four-day food deprivation. In closed incubations, C and N budgets were derived from the difference between C and N uptake during feeding and subsequent C and N loss through respiration, ammonium excretion, release of particulate organic carbon and nitrogen (POC, PON). Additional feeding with krill significantly increased coral respiration (35%), excretion (131%), and POC release (67%) compared to feeding on zooplankton only. Nevertheless, the higher C and N losses were overcompensated by the threefold higher C and N uptake, indicating a high assimilation and growth efficiency for the krill plus zooplankton diet. In contrast, short food deprivation caused a substantial reduction in respiration (59%), excretion (54%), release of POC (73%) and PON (87%) compared to feeding on zooplankton, suggesting a high potential to acclimatize to food scarcity (e.g., in winter). Notwithstanding, unfed corals 'lost' 2% of their tissue-C and 1.2% of their tissue-N per day in terms of metabolism and released particulate organic matter (likely mucus). To balance the C (N) losses, each D. dianthus polyp has to consume around 700 (400) zooplankters per day. The capture of a single, large krill individual, however, provides enough C and N to compensate daily C and N losses and grow tissue reserves, suggesting that krill plays an important nutritional role for the fjord corals. Efficient krill and zooplankton capture, as well as dietary and metabolic flexibility, may enable D. dianthus to thrive under adverse environmental conditions in its fjord habitat; however, it is not known how combined anthropogenic warming, acidification and eutrophication jeopardize the energy balance of this important habitat-building species.

Author Correction: Benthic fauna declined on a whitening Antarctic continental shelf.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Benthic fauna declined on a whitening Antarctic continental shelf.

Ice retreat in West Antarctica and Antarctic Peninsula has led to important changes in seafloor communities and gains in benthic blue carbon. In most of the Antarctic, however, sea ice increased between the 1970s and 2014, but its effects on the benthos remain largely unexplored. Here, we provide a 1988-2014 record of macro- and megafauna from the north-eastern Weddell Sea shelf, where benthic biomass decreased by two thirds and composition shifted from suspension feeders to deposit feeders. Concomitant increases in sea-ice cover suggest a reduced flux of primary production to the benthos. As benthic communities are major repositories for Antarctic biodiversity and play an important role in biogeochemical cycling, the observed changes have far-reaching consequences for the Antarctic ecosystem and its feedback to the climate system. The findings underscore the importance of long-term ecological monitoring in a region vulnerable to warming and ice-shelf collapse.

Ciliary vortex flows and oxygen dynamics in the coral boundary layer.

The exchange of metabolites between environment and coral tissue depends on the flux across the diffusive boundary layer (DBL) surrounding the tissue. Cilia covering the coral tissue have been shown to create vortices that enhance mixing in the DBL in stagnant water. To study the role of cilia under simulated ambient currents, we designed a new light-sheet microscopy based flow chamber setup. Microparticle velocimetry was combined with high-resolution oxygen profiling in the coral Porites lutea under varying current and light conditions with natural and arrested cilia beating. Cilia-generated vortices in the lower DBL mitigated extreme oxygen concentrations close to the tissue surface. Under light and arrested cilia, oxygen surplus at the tissue surface increased to 350 µM above ambient, in contrast to 25 µM under ciliary beating. Oxygen shortage in darkness decreased from 120 µM (cilia arrested) to 86 µM (cilia active) below ambient. Ciliary redistribution of oxygen had no effect on the photosynthetic efficiency of the photosymbionts and overall oxygen flux across the DBL indicating that oxygen production and consumption was not affected. We found that corals actively change their environment and suggest that ciliary flows serve predominantly as a homeostatic control mechanism which may play a crucial role in coral stress response and resilience.

All you can eat: the functional response of the cold-water coral Desmophyllum dianthus feeding on krill and copepods.

The feeding behavior of the cosmopolitan cold-water coral (CWC) Desmophyllum dianthus (Cnidaria: Scleractinia) is still poorly known. Its usual deep distribution restricts direct observations, and manipulative experiments are so far limited to prey that do not occur in CWC natural habitat. During a series of replicated incubations, we assessed the functional response of this coral feeding on a medium-sized copepod (Calanoides patagoniensis) and a large euphausiid (Euphausia vallentini). Corals showed a Type I functional response, where feeding rate increased linearly with prey abundance, as predicted for a tentaculate passive suspension feeder. No significant differences in feeding were found between prey items, and corals were able to attain a maximum feeding rate of 10.99 mg C h-1, which represents an ingestion of the 11.4% of the coral carbon biomass per hour. These findings suggest that D. dianthus is a generalist zooplankton predator capable of exploiting dense aggregations of zooplankton over a wide prey size-range.

Pristine populations of habitat-forming gorgonian species on the Antarctic continental shelf.

Declines in the abundance of long-lived and habitat-forming species on continental shelves have attracted particular attention given their importance to ecosystem structure and function of marine habitats. The study of undisturbed habitats defined as "pristine areas" is essential in creating a frame of reference for natural habitats free of human interference. Gorgonian species are one of the key structure-forming taxa in benthic communities on the Antarctic continental shelf. Current knowledge of the diversity, distribution and demography of this group is relatively limited in Antarctica. To overcome this lack of information we present original data on pristine and remote populations of gorgonians from the Weddell Sea, some of which display the largest colony sizes ever recorded in Antarctica. We assessed the distribution patterns of seven gorgonian species, a morphogroup and a family in front of the Filchner Ronne Ice Shelf (Weddell Sea) by means of quantitative analysis of video transects. Analysis of these videos showed a total of 3140 colonies of gorgonians with the highest abundance in the southern section and a significantly clumped distribution. This study contributes to the general knowledge of pristine areas of the continental shelf and identifies the eastern Weddell Sea as a hotspot for habitat-forming species.

Pontellid copepods, Labidocera spp., affected by ocean acidification: A field study at natural CO2 seeps.

CO2 seeps in coral reefs were used as natural laboratories to study the impacts of ocean acidification on the pontellid copepod, Labidocera spp. Pontellid abundances were reduced by ∼70% under high-CO2 conditions. Biological parameters and substratum preferences of the copepods were explored to determine the underlying causes of such reduced abundances. Stage- and sex-specific copepod lengths, feeding ability, and egg development were unaffected by ocean acidification, thus changes in these physiological parameters were not the driving factor for reduced abundances under high-CO2 exposure. Labidocera spp. are demersal copepods, hence they live amongst reef substrata during the day and emerge into the water column at night. Deployments of emergence traps showed that their preferred reef substrata at control sites were coral rubble, macro algae, and turf algae. However, under high-CO2 conditions they no longer had an association with any specific substrata. Results from this study indicate that even though the biology of a copepod might be unaffected by high-CO2, Labidocera spp. are highly vulnerable to ocean acidification.

Reduced heterotrophy in the stony coral Galaxea fascicularis after life-long exposure to elevated carbon dioxide.

Ocean acidification imposes many physiological, energetic, structural and ecological challenges to stony corals. While some corals may increase autotrophy under ocean acidification, another potential mechanism to alleviate some of the adverse effects on their physiology is to increase heterotrophy. We compared the feeding rates of Galaxea fascicularis colonies that have lived their entire lives under ocean acidification conditions at natural carbon dioxide (CO2) seeps with colonies living under present-day CO2 conditions. When provided with the same quantity and composition of zooplankton as food, corals acclimatized to high CO2 showed 2.8 to 4.8 times depressed rates of zooplankton feeding. Results were consistent over four experiments, from two expeditions and both in field and chamber measurements. Unless replenished by other sources, reduced zooplankton uptake in G. fascicularis acclimatized to ocean acidification is likely to entail a shortage of vital nutrients, potentially jeopardizing their health and survival in future oceans.

Elevated temperature causes metabolic trade-offs at the whole-organism level in the Antarctic fish Trematomus bernacchii.

As a response to ocean warming, shifts in fish species distribution and changes in production have been reported that have been partly attributed to temperature effects on the physiology of animals. The Southern Ocean hosts some of the most rapidly warming regions on earth and Antarctic organisms are reported to be especially temperature sensitive. While cellular and molecular organismic levels appear, at least partially, to compensate for elevated temperatures, the consequences of acclimation to elevated temperature for the whole organism are often less clear. Growth and reproduction are the driving factors for population structure and abundance. The aim of this study was to assess the effect of long-term acclimation to elevated temperature on energy budget parameters in the high-Antarctic fish Trematomus bernacchii. Our results show a complete temperature compensation for routine metabolic costs after 9 weeks of acclimation to 4°C. However, an up to 84% reduction in mass growth was measured at 2 and 4°C compared with the control group at 0°C, which is best explained by reduced food assimilation rates at warmer temperatures. With regard to a predicted temperature increase of up to 1.4°C in the Ross Sea by 2200, such a significant reduction in growth is likely to affect population structures in nature, for example by delaying sexual maturity and reducing production, with severe impacts on Antarctic fish communities and ecosystems.

Coral growth and bioerosion of Porites lutea in response to large amplitude internal waves.

The Similan Islands (Thailand) in the Andaman Sea are exposed to large amplitude internal waves (LAIW), as evidenced by i.a. abrupt fluctuations in temperature of up to 10°C at supertidal frequencies. Although LAIW have been shown to affect coral composition and framework development in shallow waters, the role of LAIW on coral growth is so far unknown. We carried out a long-term transplant experiment with live nubbins and skeleton slabs of the dominating coral Porites lutea to assess the net growth and bioerosion in LAIW-exposed and LAIW-protected waters. Depth-related, seasonal and interannual differences in LAIW-intensities on the exposed western sides of the islands allowed us to separate the effect of LAIW from other possible factors (e.g. monsoon) affecting the corals. Coral growth and bioerosion were inversely related to LAIW intensity, and positively related to coral framework development. Accretion rates of calcareous fouling organisms on the slabs were negligible compared to bioerosion, reflecting the lack of a true carbonate framework on the exposed W faces of the Similan Islands. Our findings show that LAIW may play an important, yet so far overlooked, role in controlling coral growth in tropical waters.

Benthic reef primary production in response to large amplitude internal waves at the Similan Islands (Andaman Sea, Thailand).

Coral reefs are facing rapidly changing environments, but implications for reef ecosystem functioning and important services, such as productivity, are difficult to predict. Comparative investigations on coral reefs that are naturally exposed to differing environmental settings can provide essential information in this context. One prevalent phenomenon regularly introducing alterations in water chemistry into coral reefs are internal waves. This study therefore investigates the effect of large amplitude internal waves (LAIW) on primary productivity in coral reefs at the Similan Islands (Andaman Sea, Thailand). The LAIW-exposed west sides of the islands are subjected to sudden drops in water temperature accompanied by enhanced inorganic nutrient concentrations compared to the sheltered east. At the central island, Ko Miang, east and west reefs are only few hundred meters apart, but feature pronounced differences. On the west lower live coral cover (-38 %) coincides with higher turf algae cover (+64 %) and growth (+54 %) compared to the east side. Turf algae and the reef sand-associated microphytobenthos displayed similar chlorophyll a contents on both island sides, but under LAIW exposure, turf algae exhibited higher net photosynthesis (+23 %), whereas the microphytobenthos displayed reduced net and gross photosynthesis (-19 % and -26 %, respectively) accompanied by lower respiration (-42 %). In contrast, the predominant coral Porites lutea showed higher chlorophyll a tissues contents (+42 %) on the LAIW-exposed west in response to lower light availability and higher inorganic nutrient concentrations, but net photosynthesis was comparable for both sides. Turf algae were the major primary producers on the west side, whereas microphytobenthos dominated on the east. The overall primary production rate (comprising all main benthic primary producers) was similar on both island sides, which indicates high primary production variability under different environmental conditions.

Vertical and horizontal distribution of Desmophyllum dianthus in Comau Fjord, Chile: a cold-water coral thriving at low pH.

Cold-water corals provide an important habitat for a rich fauna along the continental margins and slopes. Although these azooxanthellate corals are considered particularly sensitive to ocean acidification, their responses to natural variations in pH and aragonite saturation are largely unknown due to the difficulty of studying their ecology in deep waters. Previous SCUBA investigations have shown an exceptionally shallow population of the cold-water coral Desmophyllum dianthus in near-surface waters of Comau Fjord, a stratified 480 m deep basin in northern Chilean Patagonia with suboxic deep waters. Here, we use a remotely operated vehicle to quantitatively investigate the distribution of D. dianthus and its physico-chemical drivers in so far uncharted naturally acidified waters. Remarkably, D. dianthus was ubiquitous throughout the fjord, but particularly abundant between 20 and 280 m depth in a pH range of 8.4 to 7.4. The persistence of individuals in aragonite-undersaturated waters suggests that present-day D. dianthus in Comau Fjord may show pre-acclimation or pre-adaptation to conditions of ocean acidification predicted to reach over 70% of the known deep-sea coral locations by the end of the century.