The Gill Microbiota of Argopecten purpuratus Scallop Is Dominated by Symbiotic Campylobacterota and Upwelling Intensification Differentially Affects Their Abundance.

Despite the great importance of gills for bivalve mollusks (respiration, feeding, immunity), the microbiota associated with this tissue has barely been characterized in scallops. The scallop Argopecten purpuratus is an important economic resource that is cultivated in areas where coastal upwelling is intensifying by climate change, potentially affecting host-microbiota interactions. Thus, we first characterized the bacterial community present in gills from cultivated scallops (by 16S rRNA gene amplicon sequencing) and assessed their stability and functional potential in animals under farm and laboratory conditions. Results showed that under both conditions the gill bacterial community is dominated by the phylum Campylobacterota (57%), which displays a chemoautotrophic potential that could contribute to scallop nutrition. Within this phylum, two phylotypes, namely symbionts A and B, were the most abundant; being, respectively, taxonomically affiliated to symbionts with nutritional functions in mussel gills, and to uncultured bacteria present in coral mucus. Additionally, in situ hybridization and scanning electron microscopy analyses allowed us to detect these symbionts in the gills of A. purpuratus. Given that shifts in upwelling phenology can cause disturbances to ecosystems, affecting bacteria that provide beneficial functions to the host, we further assessed the changes in the abundance of the two symbionts (via qPCR) in response to a simulated upwelling intensification. The exposure to combined decreasing values in the temperature, pH, and oxygen levels (upwelling conditions) favored the dominance of symbiont B over symbiont A; suggesting that symbiont abundances are modulated by these environmental changes. Overall, results showed that changes in the main Campylobacterota phylotypes in response to upwelling intensification could affect its symbiotic function in A. purpuratus under future climate change scenarios. These results provide the first insight into understanding how scallop gill-microbial systems adapt and respond to climate change stressors, which could be critical for managing health, nutrition, and scallop aquaculture productivity.

Trace elements in Antarctic penguins and the potential role of guano as source of recycled metals in the Southern Ocean.

Penguins dominate the Antarctic avifauna. As key animals in the Antarctic ecosystem, they are monitored to evaluate the ecological status of this pristine and remote region and specifically, they have been used as effective bioindicators suitable for long-term monitoring of metals in the Antarctic environment. However, studies about the role of this emblematic organism could play in the recycling of trace metals (TMs) in the Antarctic ecosystem are very limited. In this study we evaluate, using the peer review research articles already published and our own findings, the distribution of metals (i.e., Ca, Fe, Al, Na, Zn, Mg, Cu, K, Cd, Mn, Sr, Cr, Ni, Pb, Hg, V, Ba, Co, La, Ag, Rb, Hf, Sc, Au and Cs) and metalloids (As and Sb), measured in different biotic matrices, with emphasis on guano, of the Chinstrap (Pygoscelis antarcticus), Adélie (Pygoscelis adeliae) and Gentoo (Pygoscelis papua) penguins. Regarding bioactive metals, the high concentrations (µg g-1 dry weight) of Cu (2.0 ± 1.4) x 102, Fe (4.1 ± 2.9) x 102, Mn (30 ± 34) and Zn (210 ± 90) reported in the guano from all the penguin species studied including our data, are of the same order of magnitude as those reported for whale feces (µg g-1 dry weight): Cu (2.9 ± 2.4) x 102, Fe (1.5 ± 1.4) x 102, Mn (28 ± 17) and Zn (6.2 ± 4.3) x 102, and one order of magnitude higher than the metal contents in krill (µg g-1 dry weight) of Cu (10.2 ± 5.5), Fe (24 ± 29) and Zn (13.5 ± 1.7). This suggest that penguin's excretion products could be an important source of these essential elements in the surface water, with an estimated annual release on a breeding season for Cu, Fe, Mn, Zn respectively of 28, 56, 4 and 29 tons, for the Chinstrap, Adélie and Gentoo penguins. The results provide evidence on the potential influence of penguins recycling TMs in the surface layer of the water column.

Upwelling intensity modulates the fitness and physiological performance of coastal species: Implications for the aquaculture of the scallop Argopecten purpuratus in the Humboldt Current System.

Understanding how marine species cope with the natural environmental variability of their native habitats will provide significant information about their sensitivity to the potential environmental changes driven by climate change. In particular, marine species inhabiting upwelling ecosystems are experiencing low seawater temperatures, as well as, acidic and low oxygen conditions as a consequence of the nature of the deep upwelled waters. Our study is focused on one of the most important socio-economical resources of the Humboldt Current System (HCS): the scallop Argopecten purpuratus which has been historically subjected to intensive aquaculture in areas influenced by upwelling processes. Here, a long-term field experiment was performed to understand how tolerant and well-locally-adapted is A. purpuratus to upwelling conditions by studying a set of fitness, physiological, and biomineralogical traits. Stronger upwelling generated a minor water column stratification, with lower temperatures, pH, and oxygen conditions. On the contrary, as upwelling weakened, temperature, pH, and oxygen availability increased. Finally, upwelling intensity also determined the number, duration, and intensity of the cooling and de-oxygenation events occurring in A. purpuratus habitat, as well as, the food availability (chlorophyll-a concentration, Chl-a). Physiologically, A. purpuratus was able to cope with stressful environmental conditions imposed by higher upwelling intensities by enhancing its metabolic and calcification rates, as well, producing higher concentrations of the shell organic matter. These physiological changes impacted the total energy budget, which was highly dependent on Chl-a concentration, and revealed important traits trade-offs with significant fitness costs (higher mortalities emerged when longer and more intense upwelling events succeed). Our study increases the knowledge about the physiological performance and tolerance of this important resource to the ocean acidification and ocean-deoxygenation imposed by variable upwelling intensities, as well as, its potential vulnerability under future changing conditions driven by a potential upwelling intensification.

The combined effects of salinity and pH on shell biomineralization of the edible mussel Mytilus chilensis.

Coastal ecosystems influenced by river discharges are subjected to important environmental changes. Understanding how marine biota cope with its environment is relevant in predicting the responses to future conditions imposed by climate change. To date, a large number of studies have addressed the role of pH on shell and biomineralization properties on multiple calcifying species; however the role of salinity in combination with other stressors has been poorly studied. In particular, the edible mussel Mytilus chilensis, an important marine resource of the Chilean coasts, inhabits estuarine areas which show high natural variability in terms of pH and salinity. Here, we studied how M. chilensis shell periostracum, shell organic matrix and crystal orientation are affected by different pH (8.1 and 7.7) and salinity conditions (30, 25 and 20 psu), isolated and in combination, at different time intervals. Our results show differences in the plasticity of the different biomineralogical properties studied during the experiment under the different pH and salinity treatments. While the periostracum thickness and the total shell organic matter were not affected by pH and salinity, the periostracum organic composition did. Higher amounts of polysaccharides were observed under low pH conditions after 20 days of experiment, while after 60 days, low salinity was responsible for the decrease of the polysaccharides and proteins in the periostracum. Low salinity also produced a major disorder in crystal organization at the outer shell surface. Finally, total shell weight was only affected by low pH conditions under lower salinity conditions (20 psu). From the results, in the majority of the shell properties observed we did not observe any combined effect of pH and salinity. Also, we detected that the magnitude of the impacts of salinity and pH are variable and time-dependent. This would be suggesting some level of acclimatization of M. chilensis to lower pH and salinity conditions.

Seagrass Posidonia oceanica diel pH fluctuations reduce the mortality of epiphytic forams under experimental ocean acidification.

It is hypothesized that pH fluctuations produced by seagrasses metabolism may confer marine calcifiers resistance to ocean acidification. Here, we tested this thesis by comparing the net population growth rate (NPGR) of a foraminifer species (Rosalina sp.) epiphytic of Mediterranean seagrass (Posidonia oceanica) to average current and projected pH scenarios under either stable conditions or diel fluctuations in pH of 0.3 units; variations similar to that experienced in their habitat. No significant differences were found in NPGRs between the fluctuating and stable pH treatments at current pH levels. NPGRs in treatments where pH fluctuated did not present significant differences to the treatment with high and stable pH conditions. In contrast, foraminifers exposed to stable low pH regimes experienced a steep decline in NPGR. These results suggest that diel pH fluctuations generated by P. oceanica photosynthetic activity could confer resistance to ocean acidification to Rosalina sp.

Reply to 'Increased food supply mitigates ocean acidification effects on calcification but exacerbates effects on growth'.

In the Brown et al. study 'Increased food supply mitigates ocean acidification effects on calcification but exacerbates effects on growth' they show disagreement with the tested hypothesis and data analysis methodology used in our 2016 study. We acknowledge careful criticism and a constructive dialogue are necessary to progress science and address these issues in this reply.Replying to: Brown et al. Sci. Rep. 8 (2018); https://doi.org/10.1038/s41598-018-28012-w .

Seagrass (Posidonia oceanica) seedlings in a high-CO2 world: from physiology to herbivory.

Under future increased CO2 concentrations, seagrasses are predicted to perform better as a result of increased photosynthesis, but the effects in carbon balance and growth are unclear and remain unexplored for early life stages such as seedlings, which allow plant dispersal and provide the potential for adaptation under changing environmental conditions. Furthermore, the outcome of the concomitant biochemical changes in plant-herbivore interactions has been poorly studied, yet may have important implications in plant communities. In this study we determined the effects of experimental exposure to current and future predicted CO2 concentrations on the physiology, size and defense strategies against herbivory in the earliest life stage of the Mediterranean seagrass Posidonia oceanica. The photosynthetic performance of seedlings, assessed by fluorescence, improved under increased pCO2 conditions after 60 days, although these differences disappeared after 90 days. Furthermore, these plants exhibited bigger seeds and higher carbon storage in belowground tissues, having thus more resources to tolerate and recover from stressors. Of the several herbivory resistance traits measured, plants under high pCO2 conditions had a lower leaf N content but higher sucrose. These seedlings were preferred by herbivorous sea urchins in feeding trials, which could potentially counteract some of the positive effects observed.

Food supply confers calcifiers resistance to ocean acidification.

Invasion of ocean surface waters by anthropogenic CO2 emitted to the atmosphere is expected to reduce surface seawater pH to 7.8 by the end of this century compromising marine calcifiers. A broad range of biological and mineralogical mechanisms allow marine calcifiers to cope with ocean acidification, however these mechanisms are energetically demanding which affect other biological processes (trade-offs) with important implications for the resilience of the organisms against stressful conditions. Hence, food availability may play a critical role in determining the resistance of calcifiers to OA. Here we show, based on a meta-analysis of existing experimental results assessing the role of food supply in the response of organisms to OA, that food supply consistently confers calcifiers resistance to ocean acidification.

Biomineralization changes with food supply confer juvenile scallops (Argopecten purpuratus) resistance to ocean acidification.

Future ocean acidification (OA) will affect physiological traits of marine species, with calcifying species being particularly vulnerable. As OA entails high energy demands, particularly during the rapid juvenile growth phase, food supply may play a key role in the response of marine organisms to OA. We experimentally evaluated the role of food supply in modulating physiological responses and biomineralization processes in juveniles of the Chilean scallop, Argopecten purpuratus, that were exposed to control (pH ~ 8.0) and low pH (pH ~ 7.6) conditions using three food supply treatments (high, intermediate, and low). We found that pH and food levels had additive effects on the physiological response of the juvenile scallops. Metabolic rates, shell growth, net calcification, and ingestion rates increased significantly at low pH conditions, independent of food. These physiological responses increased significantly in organisms exposed to intermediate and high levels of food supply. Hence, food supply seems to play a major role modulating organismal response by providing the energetic means to bolster the physiological response of OA stress. On the contrary, the relative expression of chitin synthase, a functional molecule for biomineralization, increased significantly in scallops exposed to low food supply and low pH, which resulted in a thicker periostracum enriched with chitin polysaccharides. Under reduced food and low pH conditions, the adaptive organismal response was to trade-off growth for the expression of biomineralization molecules and altering of the organic composition of shell periostracum, suggesting that the future performance of these calcifiers will depend on the trajectories of both OA and food supply. Thus, incorporating a suite of traits and multiple stressors in future studies of the adaptive organismal response may provide key insights on OA impacts on marine calcifiers.

Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming.

Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity, despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusk larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting that it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single-species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature.