Shell disease does not affect biochemical profiles of the North Sea brown shrimp Crangon crangon.

The brown shrimp Crangon crangon is a key component of the North Atlantic coastal food web and an important target species for the fishery economy. As the brown shrimp contains large amounts of protein and essential fatty acids, its consumption makes it a beneficial choice for humans. Commercially harvested crustaceans like C. crangon are frequently affected by bacterial shell disease, with necrotizing erosions and ulcerations of the cuticle. To determine whether shell disease influences the nutritional value of C. crangon, total protein and lipid contents, as well as fatty acid compositions of muscle tissue and hepatopancreas, together with the hepatosomatic index, were examined in healthy and affected individuals. The biochemical composition of the tissues did not differ significantly between the 2 groups. Also, the hepatosomatic index, as an indicator of energy reserves in shrimps, was similar between healthy and affected animals. Our results indicate that the nutritional value of C. crangon is not affected by shell disease, as long as it remains superficial as in the present study.

Functional genomic analysis of corals from natural CO2 -seeps reveals core molecular responses involved in acclimatization to ocean acidification.

Little is known about the potential for acclimatization or adaptation of corals to ocean acidification and even less about the molecular mechanisms underpinning these processes. Here, we examine global gene expression patterns in corals and their intracellular algal symbionts from two replicate population pairs in Papua New Guinea that have undergone long-term acclimatization to natural variation in pCO2 . In the coral host, only 61 genes were differentially expressed in response to pCO2 environment, but the pattern of change was highly consistent between replicate populations, likely reflecting the core expression homeostasis response to ocean acidification. Functional annotations highlight lipid metabolism and a change in the stress response capacity of corals as key parts of this process. Specifically, constitutive downregulation of molecular chaperones was observed, which may impact response to combined climate change-related stressors. Elevated CO2 has been hypothesized to benefit photosynthetic organisms but expression changes of in hospite Symbiodinium in response to acidification were greater and less consistent among reef populations. This population-specific response suggests hosts may need to adapt not only to an acidified environment, but also to changes in their Symbiodinium populations that may not be consistent among environments, adding another challenging dimension to the physiological process of coping with climate change.

Trade-offs in a reef-building coral after six years of thermal acclimation.

There is growing evidence that reef-building corals can acclimate to novel and challenging thermal conditions. However, potential trade-offs that accompany acclimation remain largely unexplored. We investigated physiological trade-offs in colonies of a globally abundant coral species (Pocillopora acuta) that were acclimated ex situ to an elevated temperature of 31 °C (i.e., 1 °C above their bleaching threshold) for six years. By comparing them to conspecifics maintained at a cooler temperature, we found that the energy storage of corals was prioritized over skeletal growth at the elevated temperature. This was associated with the formation of higher density skeletons, lower calcification rates and consequently lower skeletal extension rates, which entails ramifications for future reef-building processes, structural complexity and reef community composition. Furthermore, symbionts were physiologically compromised at 31 °C and had overall lower energy reserves, likely due to increased exploitation by their host, resulting in an overall lower stress resilience of the holobiont. Our study shows how biological trade-offs of thermal acclimation unfold, helping to refine our picture of future coral reef trajectories. Importantly, our observations in this six-year study do not align with observations of short-term studies, where elevated temperatures were often associated with the depletion of energy reserves, highlighting the importance of studying acclimation of organisms at relevant biological scales.

Physiological responses to self-induced burrowing and metabolic rate depression in the ocean quahog Arctica islandica.

Arctica islandica is the longest-lived non-colonial animal found so far, and reaches individual ages of 150 years in the German Bight (GB) and more than 350 years around Iceland (IC). Frequent burrowing and physiological adjustments to low tissue oxygenation in the burrowed state are proposed to lower mitochondrial reactive oxygen species (ROS) formation. We investigated burrowing patterns and shell water partial pressure of oxygen (P(O(2))) in experiments with live A. islandica. Furthermore, succinate accumulation and antioxidant defences were recorded in tissues of bivalves in the normoxic or metabolically downregulated state, as well as ROS formation in isolated gills exposed to normoxia, hypoxia and hypoxia/reoxygenation. IC bivalves burrowed more frequently and deeper in winter than in summer under in situ conditions, and both IC and GB bivalves remained burrowed for between 1 and 6 days in laboratory experiments. Shell water P(O(2)) was <5 kPa when bivalves were maintained in fully oxygenated seawater, and ventilation increased before animals entered the state of metabolic depression. Succinate did not accumulate upon spontaneous shell closure, although shell water P(O(2)) was 0 kPa for over 24 h. A ROS burst was absent in isolated gills during hypoxia/reoxygenation, and antioxidant enzyme activities were not enhanced in metabolically depressed clams compared with normally respiring clams. Postponing the onset of anaerobiosis in the burrowed state and under hypoxic exposure presumably limits the need for elevated recovery respiration upon surfacing and oxidative stress during reoxygenation.

Metabolic and physiological responses in tissues of the long-lived bivalve Arctica islandica to oxygen deficiency.

In Arctica islandica, a long lifespan is associated with low metabolic activity, and with a pronounced tolerance to low environmental oxygen. In order to study metabolic and physiological responses to low oxygen conditions vs. no oxygen in mantle, gill, adductor muscle and hemocytes of the ocean quahog, specimens from the German Bight were maintained for 3.5 days under normoxia (21 kPa=controls), hypoxia (2 kPa) or anoxia (0 kPa). Tissue levels of anaerobic metabolites octopine, lactate and succinate as well as specific activities of octopine dehydrogenase (ODH) and lactate dehydrogenase (LDH) were unaffected by hypoxic incubation, suggesting that the metabolism of A. islandica remains fully aerobic down to environmental oxygen levels of 2 kPa. PO(2)-dependent respiration rates of isolated gills indicated the onset of metabolic rate depression (MRD) below 5 kPa in A. islandica, while anaerobiosis was switched on in bivalve tissues only at anoxia. Tissue-specific levels of glutathione (GSH), a scavenger of reactive oxygen species (ROS), indicate no anticipatory antioxidant response takes place under experimental hypoxia and anoxia exposure. Highest specific ODH activity and a mean ODH/LDH ratio of 95 in the adductor muscle contrasted with maximal specific LDH activity and a mean ODH/LDH ratio of 0.3 in hemocytes. These differences in anaerobic enzyme activity patterns indicate that LDH and ODH play specific roles in different tissues of A. islandica which are likely to economize metabolism during anoxia and reoxygenation.

Diminished growth and vitality in juvenile Hydractinia echinata under anticipated future temperature and variable nutrient conditions.

In a warming climate, rising seawater temperatures and declining primary and secondary production will drastically affect growth and fitness of marine invertebrates in the northern Atlantic Ocean. To study the ecological performance of juvenile hydroids Hydractinia echinata we exposed them to current and predicted water temperatures which reflect the conditions in the inter- and subtidal in combination with changing food availability (high and low) in laboratory experiments. Here we show, that the interplay between temperature stress and diminished nutrition affected growth and vitality of juvenile hydroids more than either factor alone, while high food availability mitigated their stress responses. Our numerical growth model indicated that the growth of juvenile hydroids at temperatures beyond their optimum is a saturation function of energy availability. We demonstrated that the combined effects of environmental stressors should be taken into consideration when evaluating consequences of climate change. Interactive effects of ocean warming, decreasing resource availability and increasing organismal energy demand may have major impacts on biodiversity and ecosystem function.

Nitric oxide mediates metabolic functions in the bivalve Arctica islandica under hypoxia.

The free radical nitric oxide (NO) is a powerful metabolic regulator in vertebrates and invertebrates. At cellular concentrations in the nanomolar range, and simultaneously reduced internal oxygen partial pressures (pO2), NO completely inhibits cytochrome-c-oxidase (CytOx) activity and hence mitochondrial- and whole-tissue respiration. The infaunal clam Arctica islandica regulates pO2 of hemolymph and mantle cavity water to mean values of <5 kPa, even in a completely oxygen-saturated environment of 21 kPa. These low internal pO2 values support a longer NO lifespan and NO accumulation in the body fluids and can thus trigger a depression of metabolic rate in the clams. Measurable amounts of NO formation were detected in hemocyte cells (~110 pmol NO 100-1 hemocytes h-1 at 6 kPa), which was not prevented in the presence of the NO synthase inhibitor L-NAME, and in the gill filaments of A. islandica. Adding a NO donor to intact gills and tissue homogenate significantly inhibited gill respiration and CytOx activity below 10 kPa. Meanwhile, the addition of the NO-oxidation product nitrite did not affect metabolic rates. The high nitrite levels found in the hemolymph of experimental mussels under anoxia do not indicate cellular NO production, but could be an indication of nitrate reduction by facultative anaerobic bacteria associated with tissue and/or hemolymph biofilms. Our results suggest that NO plays an important role in the initiation of metabolic depression during self-induced burrowing and shell closure of A. islandica. Furthermore, NO appears to reduce mitochondrial oxygen radical formation during surfacing and cellular reoxygenation after prolonged periods of hypoxia and anoxia.

Contrasting responses of the coral Acropora tenuis to moderate and strong light limitation in coastal waters.

Coastal water quality and light attenuation can detrimentally affect coral health. This study investigated the effects of light limitation and reduced water quality on the physiological performance of the coral Acropora tenuis. Branches of individual colonies were collected in 2 m water depth at six inshore reefs at increasing distances from major river sources in the Great Barrier Reef, along a strong water quality gradient in the Burdekin and a weak gradient in the Whitsunday region. Rates of net photosynthesis, dark respiration, and light and dark calcification were determined at daily light integrals (DLI) of moderate (13.86-16.38 mol photons m-2 d-1), low (7.92-9.36 mol photons m-2 d-1) and no light (0 mol photons m-2 d-1), in both the dry season (October 2013, June 2014) and the wet season (February 2014). Along the strong but not the weak water quality gradient, rates of net photosynthesis, dark respiration and light calcification increased towards the river mouth both in the dry and the wet seasons. Additionally, a ∼50% light reduction (from moderate to low light), as often found in shallow turbid waters in the Burdekin region, reduced rates of net photosynthesis and light calcification by up to 70% and 50%. The data show the acclimation potential in A. tenuis to river derived nutrients and sediments at moderate DLI (i.e., in very shallow water). However, prolonged and frequent periods of low DLI (i.e., in deeper water, especially after high river sediment discharges) will affect the corals' energy balance, and may represent a major factor limiting the depth distribution of these corals in turbid coastal reefs.

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.

Gene expression and physiological changes of different populations of the long-lived bivalve Arctica islandica under low oxygen conditions.

The bivalve Arctica islandica is extremely long lived (>400 years) and can tolerate long periods of hypoxia and anoxia. European populations differ in maximum life spans (MLSP) from 40 years in the Baltic to >400 years around Iceland. Characteristic behavior of A. islandica involves phases of metabolic rate depression (MRD) during which the animals burry into the sediment for several days. During these phases the shell water oxygen concentrations reaches hypoxic to anoxic levels, which possibly support the long life span of some populations. We investigated gene regulation in A. islandica from a long-lived (MLSP 150 years) German Bight population and the short-lived Baltic Sea population, experimentally exposed to different oxygen levels. A new A. islandica transcriptome enabled the identification of genes important during hypoxia/anoxia events and, more generally, gene mining for putative stress response and (anti-) aging genes. Expression changes of a) antioxidant defense: Catalase, Glutathione peroxidase, manganese and copper-zinc Superoxide dismutase; b) oxygen sensing and general stress response: Hypoxia inducible factor alpha, Prolyl hydroxylase and Heat-shock protein 70; and c) anaerobic capacity: Malate dehydrogenase and Octopine dehydrogenase, related transcripts were investigated. Exposed to low oxygen, German Bight individuals suppressed transcription of all investigated genes, whereas Baltic Sea bivalves enhanced gene transcription under anoxic incubation (0 kPa) and, further, decreased these transcription levels again during 6 h of re-oxygenation. Hypoxic and anoxic exposure and subsequent re-oxygenation in Baltic Sea animals did not lead to increased protein oxidation or induction of apoptosis, emphasizing considerable hypoxia/re-oxygenation tolerance in this species. The data suggest that the energy saving effect of MRD may not be an attribute of Baltic Sea A. islandica chronically exposed to high environmental variability (oxygenation, temperature, salinity). Contrary, higher physiological flexibility and stress hardening may predispose these animals to perform a pronounced stress response at the expense of life span.

Imperceptible senescence: ageing in the ocean quahog Arctica islandica.

The ocean quahog Arctica islandica is the longest-lived of all bivalve and molluscan species on earth. Animals close to 400 years are common and reported maximum live span around Iceland is close to 400 years. High and stable antioxidant capacities are a possible strategy to slow senescence and extend lifespan and this study has investigated several antioxidant parameters and a mitochondrial marker enzyme in a lifetime range spanning from 4-200 years in the Iceland quahog. In gill and mantle tissues of 4-192 year old A. islandica, catalase, citrate synthase activity and glutathione concentration declined rapidly within the first 25 years, covering the transitional phase of rapid somatic growth and sexual maturation to the outgrown mature stages (approximately 32 years). Thereafter all three parameters kept rather stable levels for > 150 years. In contrast, superoxide dismutase activities maintained high levels throughout life time. These findings support the 'Free Radical-Rate of Living theory', antioxidant capacities of A. islandica are extraordinarily high and thus may explain the species long life span.