Posts Tagged 'multiple factors'

Life-stage specificity and cross-generational climate effects on the microbiome of a tropical sea urchin (Echinodermata: Echinoidea)

Microbes play a critical role in the development and health of marine invertebrates, though microbial dynamics across life stages and host generations remain poorly understood in most reef species, especially in the context of climate change. Here, we use a 4-year multigenerational experiment to explore microbe–host interactions under the Intergovernmental Panel on Climate Change (IPCC)-forecast climate scenarios in the rock-boring tropical urchin Echinometra sp. A. Adult urchins (F0) were exposed for 18 months to increased temperature and pCO2 levels predicted for years 2050 and 2100 under RCP 8.5, a period which encompassed spawning. After rearing F1 offspring for a further 2 years, spawning was induced, and F2 larvae were raised under current day and 2100 conditions. Cross-generational climate effects were also explored in the microbiome of F1 offspring through a transplant experiment. Using 16S rRNA gene sequence analysis, we determined that each life stage and generation was associated with a distinct microbiome, with higher microbial diversity observed in juveniles compared to larval stages. Although life-stage specificity was conserved under climate conditions projected for 2050 and 2100, we observed changes in the urchin microbial community structure within life stages. Furthermore, we detected a climate-mediated parental effect when juveniles were transplanted among climate treatments, with the parental climate treatment influencing the offspring microbiome. Our findings reveal a potential for cross-generational impacts of climate change on the microbiome of a tropical invertebrate species.

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Role of culture solution pH in balancing CO2 input and light intensity for maximising microalgae growth rate


  • Microalgae growth is governed by CO2 input and light intensity.
  • CO2 input & light intensity have an opposing impact on the culture pH.
  • Microalgae growth can be inhibited by excessive lighting or CO2 input.
  • Balancing CO2 input and light intensity is essential for CO2 fixation by microalgae.
  • CO2 fixation rate of 4.2 g/L by Scenedesmus sp. at optimised condition.


The interplay between CO2 input and light intensity is investigated to provide new insight to optimise microalgae growth rate in photobioreactors for environmental remediation, carbon capture, and biomass production. Little is known about the combined effect of carbon metabolism and light intensity on microalgae growth. In this study, carbonated water was transferred to the microalgae culture at different rates and under different light intensities for observing the carbon composition and growth rate. Results from this study reveal opposing effects from CO2 input and light intensity on the culture solution pH and ultimately microalgae growth rate. Excessive CO2 concentration can inhibit microalgae growth due to acidification caused by CO2 dissolution. While increasing light intensity can increase pH because the carboxylation process consumes photons and transfers hydrogen ions into the cell. This reaction is catalysed by the enzyme RuBisCO, which functions optimally within a specific pH range. By balancing CO2 input and light intensity, high microalgae growth rate and carbon capture could be achieved. Under the intermittent CO2 transfer mode, at the optimal condition of 850 mg/L CO2 input and 1089 μmol/m2/s light intensity, leading to the highest microalgae growth rate and carbon fixation of 4.2 g/L as observed in this study.

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Combined effects of ocean acidification and heat waves on the commercially valuable bivalve Callista chione

The increasing concentration of CO2 in the atmosphere, due to the consumption of fossil fuels, is causing climatic changes, such as ocean acidification (OA) and marine heat waves (MHW), which represent a threat for several marine species with both an ecological and economical relevance. In this study, the combined effects of OA and MHW were investigated in the bivalve Callista chione using a multibiomaker approach. In an experimental flow-through system, two pH levels (current ambient pH and ambient pH -0.4 as predicted by climate change scenarios) were combined with two temperature conditions (control, corresponding to the ambient temperature of 10°C and MHW corresponding to ambient + 7°C). The effects on immune system-related parameters (total number, morphology, and functionality of haemocytes) and oxidative stress-related parameters (catalase, acetylcholinesterase and butyrylcholinesterase activities, lipid peroxidation and antioxidant capacity), were assessed at the beginning of the experiment, at the end of the MHW and after the recovery. In general, haemocytes number and dimensions were not significantly affected by the experimental factors nor their interaction. The biochemical parameters were instead influenced by the single experimental conditions (such as temperature, pH, and exposure time), with a different pattern depending on the biomarker and the tissue analyzed. The results also demonstrated that there was not a significant interaction between ocean acidification and heat waves.

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Responses of marine trophic levels to the combined effects of ocean acidification and warming

Marine organisms are simultaneously exposed to anthropogenic stressors associated with ocean acidification and warming with likely interactive effects. Although new research has started to uncover how marine primary producers, herbivores, and predators are responding to climate change, we still do not have a comprehensive understanding of general patterns across trophic levels in response to multiple stressors. Yet, marine species from different trophic levels with dissimilar characteristics and evolutionary history are likely to respond differently to climatic stressors.Our study represents the first meta-analysis of multiple stressor studies to target comparisons of mean effects and identification of interaction types among marine trophic levels. The meta-analysis revealed a number of key results: (1) Predators are the most tolerant level in response to individual and combined effects of ocean acidification and warming; (2) synergistic interactions (16%) are less common than additive (40%) and antagonistic (44%) interactions; (3) interaction types vary among trophic levels, with the proportion of synergistic interactions decreasing with increasing trophic level; (4) for interactive effects, calcifying and non-calcifying species show similar patterns across trophic levels; and (5) trophic levels respond to stressors differently along a latitudinal gradient. This study emphasizes the importance of considering stressor interactions and trophic levels in conservation actions. Contrary to many predictions, which has suggested synergistic effects predominate multiple stressors, this research demonstrates that the interaction effect between ocean acidification (OA) and ocean warming (OW) can sometimes mitigate or even reduce negative effects, with additive and antagonistic interactions dominating. Our study provides new knowledge for understanding how multiple stressors may interactively affect marine trophic levels and highlighting the need for further research and a deeper understanding of multiple stressors in conservation efforts.

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Decreased calcification to photosynthesis ratio in coccolithophores under reduced O2 and elevated CO2 environment

We examined the physiological performance in the most cosmopolitan coccolithophorid, Emiliania huxleyi, and Gephyrocapsa oceanica, which were treated with 8.3 (AO), 4.6 (MO) and 2.5 (LO) mg L–1 O2 under 400 (AC) and1000 (HC) ppm CO2 conditions. Elevated CO2 decreased the specific growth rate of cells cultured under AO and LO conditions in both species, but it increased the rate in the MO-grown E. huxleyi. Regardless of the CO2 levels, diminished O2 concentration inhibited the growth rate in E. huxleyi while accelerating the rate in G. oceanica. LO reduced the particulate organic carbon (POC) production rate compared to the AO treatment in both species. Additionally, the decrease was higher in the HC cultures than in the AC ones. LO also inhibited the production rate of particulate inorganic carbon (PIC) compared to the AO/AC treatment. Due to a higher reduction in the production rate of PIC than POC, the PIC/POC ratio was decreased in the LO treatment compared to the AO/AC treatment. The current study reveals that low O2 can, individually or in combination with high CO2, considerably affect the physiology of marine photoautotrophic organisms.

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Direct and indirect impacts of ocean acidification and warming on algae-herbivore interactions in intertidal habitats


  • Ocean acidification (OA) and warming (OW) alter algae-herbivore interactions
  • OA and OW modify biochemical composition of the kelp Lessonia spicata.
  • Changes in kelp biochemical composition affect snail’s feeding behaviour.
  • OW and OA conditions increased snail’s metabolic stress.
  • Nutritional quality of food plays a key role on grazers’ physiological energetics.


Anthropogenically induced global climate change has caused profound impacts in the world ocean. Climate change related stressors, like ocean acidification (OA) and warming (OW) can affect physiological performance of marine species. However, studies evaluating the impacts of these stressors on algae-herbivore interactions have been much more scarce. We approached this issue by assessing the combined impacts of OA and OW on the physiological energetics of the herbivorous snail Tegula atra, and whether this snail is affected indirectly by changes in biochemical composition of the kelp Lessonia spicata, in response to OA and OW. Our results show that OA and OW induce changes in kelp biochemical composition and palatability (organic matter, phenolic content), which in turn affect snails’ feeding behaviour and energy balance. Nutritional quality of food plays a key role on grazers’ physiological energetics and can define the stability of trophic interactions in rapidly changing environments such as intertidal communities.

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Transgenerational adaptation to ocean acidification determines the susceptibility of filter-feeding rotifers to nanoplastics

The adaptation of marine organisms to the impending challenges presented by ocean acidification (OA) is essential for their future survival, and mechanisms underlying OA adaptation have been reported in several marine organisms. In the natural environment, however, marine organisms are often exposed to a combination of environmental stressors, and the interactions between adaptive responses have yet to be elucidated. Here, we investigated the susceptibility of filter-feeding rotifers to short-term (ST) and long-term (LT) (≥180 generations) high CO2 conditions coupled with nanoplastic (NPs) exposure (ST+ and LT+). Adaptation of rotifers to elevated CO2 caused differences in ingestion and accumulation of NPs, resulting in a significantly different mode of action on in vivo endpoints between the ST+ and LT+ groups. Moreover, microRNA-mediated epigenetic regulation was strongly correlated with the varied adaptive responses between the ST+ and LT+ groups, revealing novel regulatory targets and pathways. Our results indicate that pre-exposure history to increased CO2 levels is an important factor in the susceptibility of rotifers to NPs.

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Early life physiological and energetic responses of Atlantic silversides (Menidia menidia) toocean acidification, warming, and hypoxia

Global environmental change caused by human actions is making the oceans warmer, deoxygenating coastal waters, and causing acidification through dissolution of atmospheric carbon dioxide (CO2). Understanding physiological mechanisms of fish responses to multiple co-occurring stressors is critical to conservation of marine ecosystems and the fish populations they support. In this dissertation I quantified physiological impacts of near-future levels of multiple stressors in the early life stages of the Atlantic silverside, Menidia menidia. In Chapter 1, I measured routine metabolic rates of embryos and larvae reared in combinations of temperature, CO2, and oxygen levels. An interactive effect of acidification and hypoxia in embryos prompted closer examination in Chapter 2, in which I characterized the relationship between metabolism and acute hypoxia in M. menidia offspring reared in different CO2 levels. In Chapter 3 I examined the density of skin surface ionocytes, cells used for acid-base balance, as an early life mechanism of high CO2 tolerance. The first three chapters highlighted how different CO2 effects could be depending on temperature, oxygen levels, and life stage. They also showed variable, but often high, tolerance of CO2 with stronger effects of temperature and hypoxia on physiology. Finally, in Chapter 4 I used a Dynamic Energy Budget model to identify the processes of energetic allocation responsible for previously observed experimental hypoxia effects on M. menidia hatching, growth, and survival. Energy budget modeling can enhance knowledge about stressor responses by providing the information to link organismal traits to life history and populations, making it more readily applicable to conservation and management. The findings presented here provide a foundation for a more comprehensive understanding of the highly variable effects of global change on M. menidia and should be applied to quantifying impacts on fitness and population growth in this ecologically important species.

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The synergistic negative effects of combined acidification and warming on the coral host and its symbiotic association with Symbiodiniaceae indicated by RNA-Seq differential expression analysis

Global warming and ocean acidification represent major threats to coral reefs, the combination of these stressors may have concomitant impacts on coral holobionts. However, the molecular mechanisms of the impacts and synergistic effects of acidification and warming on coral holobionts are rarely known, particularly from the point of coral-Symbiodiniaceae symbioses. In this study, using branching Acropora valida and massive Galaxea fascicularis as representatives in a laboratory system simulating acidification (pH 7.7) and/or warming (32 °C), the response of coral host, Symbiodiniaceae and their symbiotic association were investigated by high-throughput transcriptome sequencing (RNA-Seq) with pH 8.1 and 26 °C as controls. Based on differentially expressed genes (DEGs) analysis, acidification and/or warming show greater impacts on the gene expression of coral host than its symbiotic Symbiodiniaceae. Synergistic effects of combined acidification and warming are suggested by comparison with single stress, especially the synergistic negative effects on coral-Symbiodiniaceae symbioses are suggested, because the expression of most of the genes related to photosynthesis, nutrient metabolism and transfer, and the symbionts recognition are downregulated indicating the instability of the coral-Symbiodiniaceae symbioses. This study provides molecular evidence for the synergy of acidification and warming on coral holobionts. In particular, the synergistic negative effects on the nutrients and symbionts recognition-based coral-Symbiodiniaceae symbioses are highlighted, which is helpful for predicting the response of coral holobionts to future global climate changes.

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Elucidating the mechanisms of stress tolerance in reef-building coral holobionts

Coral reefs worldwide are threatened by climate change effects like increasing ocean warming and ocean acidification. These increased pressures cause a dysbiosis between the coral host, algal endosymbionts, and associated coral microbiome that results in the coral host expelling algal endosymbionts, leaving the coral host with a stark white ‘bleached’ appearance. Without their endosymbionts, coral hosts are forced to sustain themselves energetically with heterotrophy instead of relying on the autotrophic carbon and energy sources that once came from the algal endosymbionts. When this response, termed ‘coral bleaching’, happens reef-wide during an extreme wave of increased ocean temperatures, this is called a mass Coral Bleaching Event. The frequency and intensity of mass Coral Bleaching events are increasing around the world, forcing corals to acclimatize to survive. This dissertation investigates the physiological and genomic mechanisms underlying acclimatization and increased stress tolerance in two common, reef-building corals: Montipora capitata and Pocillopora acuta. In three chapters, I present findings that support phenotypic plasticity and increased stress tolerance in M. capitata and hypothesize the mechanisms contributing to this. In Chapter 1, I conducted an ex-situ experiment that mimicked an environmentally realistic, extended heatwave and ocean acidification scenario in a factorial design of increased temperature and increased pCO2 conditions for a two-month stress period and a two-month recovery period. Both species’ physiological states were significantly challenged but M. capitata displayed a more favorable photosynthetic rate to antioxidant capacity ratio and associated with more thermally tolerant symbionts. Although M. capitata survived at higher rates than P. acuta, physiological state was still significantly impacted after two months of recovery, suggesting that marine heatwaves likely induce physiological legacies that may impact performance during the next, inevitable heatwave. In Chapter 2, I further investigated P. acuta’s stress response from Chapter 1 at a genomic level. We sought to test the effects of environmental stressors on gene body DNA methylation patterns to elucidate how environmentally sensitive and dynamic DNA methylation changes are in invertebrates. However, when analyzing gene expression data, our team found that polyploidy was prevalent in our samples, which convoluted our ability to test environmental effect in addition to polyploidy structure. We found that DNA methylation patterns followed polyploidy genetic lineage with diploid corals exhibiting the highest levels of DNA methylation despite lower gene expression levels of epigenetic machinery proteins. Despite significant DNA methylation pattern differences between polyploidies, P. acuta populations still severely declined in increased stress conditions (outlined in Chapter 1), suggesting that regardless of differential gene body methylation and ploidy status, this species may be ultimately too sensitive to future ocean conditions. In Chapter 3, I further investigated the genomic mechanisms underlying stress response in Montipora capitata, by directly comparing bleached (‘Susceptible’) and non-bleached (‘Resistant’) phenotypes of conspecific pairs. We found very little genetic diversity among our samples suggesting there is no effect of genetic structure on phenotypic variation in this context. ‘Resistant’ corals were characterized by association with more thermally tolerant symbionts, lower gene expression variability, higher gene body methylation levels on genes involved in death and stress response, and a more robust cellular stress response. The results of all three chapters suggest that both physiological and genomic stats impact bleaching susceptibility and phenotype and that not one mechanism may act alone to produce a particular phenotype. This dissertation aids in elucidating the mechanisms of stress response in reef-building corals, ultimately guiding our current knowledge of phenotypic variation in the face of climate change.

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Ocean acidification affects the response of the coastal coccolithophore Pleurochrysis carterae to irradiance

The ecologically important marine phytoplankton group coccolithophores have a global distribution. The impacts of ocean acidification on the cosmopolitan species Emiliania huxleyi have received much attention and have been intensively studied. However, the species-specific responses of coccolithophores and how these responses will be regulated by other environmental drivers are still largely unknown. To examine the interactive effects of irradiance and ocean acidification on the physiology of the coastal coccolithophore species Pleurochrysis carterae, we carried out a semi-continuous incubation experiment under a range of irradiances (50, 200, 500, 800 μmol photons m−2 s−1) at two CO2 concentration conditions of 400 and 800 ppm. The results suggest that the saturation irradiance for the growth rate was higher at an elevated CO2 concentration. Ocean acidification weakened the particulate organic carbon (POC) production of Pleurochrysis carterae and the inhibition rate was decreased with increasing irradiance, indicating that ocean acidification may affect the tolerating capacity of photosynthesis to higher irradiance. Our results further provide new insight into the species-specific responses of coccolithophores to the projected ocean acidification under different irradiance scenarios in the changing marine environment.

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Impacts of ocean warming and acidification on predator-prey interactions in the intertidal zone: a research weaving approach

The effect of ocean warming and acidification on predator-prey interactions in the intertidal zone is a topic of growing concern for the scientific community. In this review, we aim to describe how scientists have explored the topic via research weaving, a combination of a systematic review, and a bibliometric approach. We assess articles published in the last decade exploring the impact of both stressors on predation in the intertidal zone, via experimental or observational techniques. Several methods were used to delve into how climate change-induced stress affected intertidal predation, as the study design leaned toward single-based driver trials to the detriment of a multi-driver approach. Mollusks, echinoderms, and crustaceans have been extensively used as model organisms, with little published data on other invertebrates, vertebrates, and algae taxa. Moreover, there is a strong web of co-authoring across institutions and countries from the Northern Hemisphere, that can skew our understanding towards temperate environments. Therefore, institutions and countries should increase participation in the southern hemisphere networking, assessing the problems under a global outlook. Our review also addresses the various impacts of ocean acidification, warming, or their interaction with predation-related variables, affecting organisms from the genetic to a broader ecological scope, such as animal behaviour or interspecific interactions. Finally, we argue that the numerous synonyms used in keywording articles in the field, possibly hurting future reviews in the area, as we provide different keyword standardizations. Our findings can help guide upcoming approaches to the topic by assessing what has been already done and revealing gaps in emerging themes, like a strong skew towards single-driver (specially acidification) lab experiments of northern hemisphere organisms and a lack of field multi-stressor experiments.

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Simultaneous warming and acidification limit population fitness and reveal phenotype costs for a marine copepod

Phenotypic plasticity and evolutionary adaptation allow populations to cope with global change, but limits and costs to adaptation under multiple stressors are insufficiently understood. We reared a foundational copepod species, Acartia hudsonica, under ambient (AM), ocean warming (OW), ocean acidification (OA), and combined ocean warming and acidification (OWA) conditions for 11 generations (approx. 1 year) and measured population fitness (net reproductive rate) derived from six life-history traits (egg production, hatching success, survival, development time, body size and sex ratio). Copepods under OW and OWA exhibited an initial approximately 40% fitness decline relative to AM, but fully recovered within four generations, consistent with an adaptive response and demonstrating synergy between stressors. At generation 11, however, fitness was approximately 24% lower for OWA compared with the AM lineage, consistent with the cost of producing OWA-adapted phenotypes. Fitness of the OWA lineage was not affected by reversal to AM or low food environments, indicating sustained phenotypic plasticity. These results mimic those of a congener, Acartia tonsa, while additionally suggesting that synergistic effects of simultaneous stressors exert costs that limit fitness recovery but can sustain plasticity. Thus, even when closely related species experience similar stressors, species-specific costs shape their unique adaptive responses.

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Response of foraminifera Ammonia confertitesta (T6) to ocean acidification, warming, and deoxygenation – an experimental approach

Ocean acidification, warmer temperatures, and the expansion of hypoxic zones in coastal areas are direct consequences of the increase in anthropogenic activities. However, so far, the combined effects of these stressors on calcium carbonate-secreting marine microorganisms – foraminifera are complex and poorly understood. This study reports the foraminiferal survival behavior, and geochemical trace elements incorporation measured from the shells of living cultured benthic foraminifera from the Gullmar fjord (Sweden) after exposure to warming, acidification, and hypoxic conditions. An experimental set-up was designed with two different temperatures (fjord’s in-situ 9 ˚C and 14 ˚C), two different oxygen concentrations (oxic versus hypoxic), and three different pH (control, medium, and low pH based on the IPCC scenario for the year 2100). Duplicate aquariums, meaning aquariums displaying the same conditions and same number of species, were employed for the controls and the two lower pH conditions at both temperatures. The stability of the aquariums was ensured by regular measurement of the water parameters and confirmed by statistical analysis. The species Ammonia confertitesta’s (T6) survival (CTB-labeled), shell calcification (calcein-labeled), and geochemical analyses (laser-ablation ICP-MS) were investigated at the end of the experimental period (48 days). Investigated trace elements (TE) ratios were Mg/Ca, Mn/Ca, Ba/Ca, and Sr/ Ca. Results show that A. confertitesta (T6) calcified chambers in all the experimental conditions except for the most severe combination of stressors (i.e., warm, hypoxic, low pH). Survival rates varied by up to a factor of two between duplicates for all conditions suggesting that foraminiferal response may not solely be driven by environmental conditions but also by internal or confounding factors (e.g., physiological stress). A large variability of all the TE/Ca values of foraminifera growing at low pH is observed suggesting that A. confertitesta (T6) may struggle to calcify in these conditions. Thus, this study demonstrates the vulnerability of a resilient species to the triple-stressor scenario in terms of survival, calcification, and trace element incorporation. Overall, the experimental set-up yielded coherent results compared to previous studies in terms of ontogeny, trace elements ratios, and partition coefficient making it advantageous for environmental reconstructions. 

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Experimental ocean acidification and food limitation reveals altered energy budgets and synergistic effects on mortality of larvae of a coastal fish

Ocean acidification (OA) presents a unique challenge to early life stages of marine species. Developing organisms must balance the need to grow rapidly with the energetic demands of maintaining homeostasis. The small sizes of early life stages can make them highly sensitive to changes in environmental CO2 levels, but studies have found wide variation in responses to OA. Thus far most OA studies have manipulated CO2 only, and modifying factors need to be considered in greater detail. We investigated the effects of high pCO2 and food ration on rates of growth and mortality of a coastal fish, the California Grunion (Leuresthes tenuis). We also examined how CO2 and food levels affected feeding success, metabolic rate, and swimming activity – processes reflective of energy acquisition and expenditure. In general, exposure to high CO2 decreased energy intake by reducing feeding success, and increased energy expenditure by increasing metabolic rate and routine swimming speed, though the magnitudes of these effects varied somewhat with age. Despite these changes in energetics, growth of biomass was not affected significantly by pCO2 level but was reduced by low ration level, and we did not detect an interactive effect of food ration and pCO2 on growth. However, under OA conditions, larvae were in poorer condition (as evaluated by the mass to length ratio) by the end of the experiment and our analysis of mortality revealed a significant interaction in which the effects of OA were more lethal when food energy was limited. These results are consistent with the idea that although energy can be reallocated to preserve biomass growth, increased energetic demand under ocean acidification may draw energy away from maintenance, including those processes that foster homeostasis during development. Overall, these results highlight both the need to consider the availability of food energy as a force governing species’ responses to ocean acidification and the need to explicitly consider the energy allocated to both growth and maintenance as climate changes.

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Effects of pH and salinity on survival, growth, and enzyme activities in juveniles of the sunray surf clam (Mactra chinensis Philippi)


  • Salinity and pH tolerance ranges were identified for Mactra chinensis Philippi juveniles in laboratory tests.
  • Survival rates were significantly reduced at extreme pH and salinity.
  • Low pH and salinity induced oxidative stress, decreasing antioxidant enzyme activities.


The study investigated the impact of salinity and pH changes on the survival, growth, and antioxidant enzyme activity in Mactra chinensis Philippi (1.00 ± 0.10 cm shell length, 0.75±0.04 cm shell height), a marine clam species. Juveniles were exposed to various pH levels (5.4 – 9.6) and salinities (5 – 35 psu) for up to 20 days at 19 ± 0.5 ˚C. The individual effect of salinity and pH on juveniles were evaluated under pH 8.0 and salinity 30 psu, respectively. The results indicated that the highest survival rates were observed at pH 8.0 (85%, salinity = 30 psu) and salinity 30 psu (95%, pH = 8.0). The survival rates were significantly reduced at extreme pH (≤ 7.2; ≥ 8.4) and salinities (≤ 15; 35 psu). Additionally, oxidative stress was observed in clams exposed to low pH and salinity as indicated by the decreased activities of the antioxidant enzymes catalase (CAT) and superoxide dismutase (SOD). Notably, no significant difference in relative growth rates was observed between salinity 25 and 30 psu, between pH 7.8/8.4 and pH 8.0. Our results provide information on potential impact of pH and salinity changes on economically important bivalve species and may be used to optimize pH and salinity in aquaculture.

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Long-term preconditioning of the coral Pocillopora acuta does not restore performance in future ocean conditions

There is overwhelming evidence that tropical coral reefs are severely impacted by human induced climate change. Assessing the capability of reef-building corals to expand their tolerance limits to survive projected climate trajectories is critical for their protection and management. Acclimation mechanisms such as developmental plasticity may provide one means by which corals could cope with projected ocean warming and acidification. To assess the potential of preconditioning to enhance thermal tolerance in the coral Pocillopora acuta, colonies were kept under three different scenarios from settlement to 17 months old: present day (0.9 °C-weeks (Degree Heating Weeks), + 0.75 °C annual, 400 ppm pCO2) mid-century (2.5 °C-weeks, + 1.5 °C annual, 685 ppm pCO2) and end of century (5 °C-weeks, + 2 °C annual, 900 ppm pCO2) conditions. Colonies from the present-day scenario were subsequently introduced to the mid-century and end of century conditions for six weeks during summer thermal maxima to examine if preconditioned colonies (reared under these elevated conditions) had a higher physiological performance compared to naive individuals. Symbiodiniaceae density and chlorophyll a concentrations were significantly lower in mid-century and end of century preconditioned groups, and declines in symbiont density were observed over the six-week accumulated heat stress in all treatments. Maximum photosynthetic rate was significantly suppressed in mid-century and end of century preconditioned groups, while minimum saturating irradiances were highest for 2050 pre-exposed individuals with parents originating from specific populations. The results of this study indicate preconditioning to elevated temperature and pCO2 for 17 months did not enhance the physiological performance in P. acuta. However, variations in trait responses and effects on tolerance found among treatment groups provides evidence for differential capacity for phenotypic plasticity among populations which could have valuable applications for future restoration efforts.

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From individual to ecosystem: multi-stressor effects of acidification and warming on the physiological responses of coastal marine invertebrates

Climate change is directly impacting the services humans derive from the sea at an accelerated rate. Ocean warming and acidification (i.e., a decrease in ocean pH) are leading to modifications in population sizes and ecosystem functioning. The observed shifts in these higher order processes are a direct result of individuals’ responses (i.e., physiology, including metabolism, growth, calcification, and survival) occurring within communities. Natural variation in past environmental exposure experienced by individuals may lead to greater population resilience, or it may push individuals past physiological thresholds leading to increased sensitivity and vulnerability to climate change. Thus, we need to determine how individual-level physiological responses to climate change scale up to influence marine ecosystems. Rocky intertidal habitats are an ideal study system for evaluating the relationships between individual physiological responses, ecosystem functioning, and climate change. Tide pools possess unique thermal and pH environments and can be monitored under natural conditions or manipulated with field-experiments over daily and seasonal time scales, creating natural “experimental mesocosms”. In addition, many species within rocky intertidal habitats are exposed to environmental conditions close to their tolerance limits, increasing their potential vulnerability to climate change. In Chapter 1, by utilizing the unique thermal environments of tide pools, I showed that across small spatial scales (pools), thermal history influences thermal sensitivity of marine invertebrates for short-term time intervals (1-week and 1-day) and that this relationship differs seasonally and between species with differing traits, including mobility. This suggests that variability in thermal responses among individuals may allow for a natural buffer at a population level in response to climate change. Multiple stressors may affect individuals independently or interactively, amplifying or mitigating effects. Thus, to determine the impacts of climate change, in Chapter 2, I used a 6-month long field manipulation of ocean warming and acidification in tide pools. I examined the combined effects of warming and acidification on the shell structure (shell thickness and corrosion) and functional properties (shell strength) of the ecologically critical species, the Pacific blue mussel (Mytilus trossulus). Acidification led to thinner, weaker, and more corroded shells whereas combined warming and acidification resulted in an increase in shell strength. My results suggest that to some degree, warming may mitigate the negative impacts of acidification on this mollusk species. Lastly, in Chapter 3, I characterize how warming and acidification, individually and interactively, impact net ecosystem calcification and the individual and population-level mechanisms driving impacts on net ecosystem calcification. Net ecosystem calcification tended to increase during the day and decrease at night; however, addition of CO2 during the hottest months led to decreased net ecosystem calcification and increased dissolution during both day and night. I found that individual mussel metabolic rates increased significantly in the presence of elevated CO2 and increased daily maximum of pool temperatures. Through this individual-level pathway, pH and temperature had a strong impact on the metabolic rates of individuals ultimately resulting in changes in net ecosystem calcification. On the other hand, greater mussel abundance was associated with increased net ecosystem calcification. Yet, with the addition of CO2, calcification decreased even in pools with the highest abundance of mussels, indicating that there are other pathways by which changes in pH can drive alterations in net ecosystem calcification. My dissertation reveals how species’ traits and natural thermal variation from short-term to seasonal time scales influence metabolic sensitivity to future warming among individuals (Ch. 1), independent climate stressors can negatively impact shellfish in situ, whereas the combined interactive effects between multiple stressors can lead to mitigation of the negative impacts of a single stressor alone (Ch. 2), and that ecosystem-level consequences of climate change are mediated by the abundance of dominant calcifiers and that this effect is dependent on the magnitude of acidification and warming (Ch. 3).

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How does ocean acidification affect Zostera marina during a marine heatwave?


  • Under extreme conditions Z. marina grows in both leaf length and wet mass.
  • Increasing CO2 levels for Z. marina at high temperatures may stimulate growth.
  • Extremely high temperatures inhibit sucrose and starch synthesis in Z. marina.
  • Out of 223 identified differentially expressed genes 70 were upregulated.
  • Glycolysis and the TCA cycle controlling genes and metabolites were upregulated.


Extreme ocean events caused by global warming, such as marine heatwaves (MHWs) and ocean acidification (OA), are projected to intensify. A combination of extreme events may have severe consequences for marine ecosystemsZostera marina was selected to understand how seagrass adapts to OA in extremely hot conditions. By combining morphology, transcriptomics, and metabolomics under mesoscale experimental conditions, we systematically investigated the response characteristics of Z. marina. Extremely high temperatures had a pronounced effect on growth, and the combined effect of OA mitigated the inhibitory effect of MHW. Both transcriptomic and metabolomic results showed that Z. marina resisted OA and MHW by upregulating the TCA cycle, glycolysis, amino acid metabolism, and relevant genes, as well as by activating the antioxidant system. The results of this study serve to improve our understanding of dual effects of factors of climate change on seagrass and may be used to direct future management and conservation efforts.

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Brown seaweed Nemacystus decipiens intensifies the effects of ocean acidification on coral Montipora digitata

Photosynthetic marine macrophytes such as seaweeds have been proposed to provide habitat refugia for marine calcifiers against ocean acidification (OA) by increasing the local pH. However, the effectiveness of seaweed as a potential habitat refugia for marine calcifiers such as corals remains to be investigated. This study focused on the seaweed Nemacystus decipiens, which are widely farmed in the shallow reef lagoon of Okinawa coral reefs, Japan, and aimed to evaluate their response to high pCO2 and whether they can mitigate the effect of high pCO2 on the coral Montipora digitata. Corals were cultured with and without seaweed under control (300–400 μatm) or high pCO2 conditions (OA, 900–1000 μatm) for 2 weeks. Results showed that all photo-physiological parameters examined in the seaweed N. decipiens were not affected by high pCO2, suggesting that OA will not positively affect their productivity. The calcification rate of the coral M. digitata was found to decrease under OA and the effect was further exaggerated by the presence of seaweed. The present study suggests that farming seaweeds will not act as a potential habitat refugia for adjacent corals under future OA, but instead can exaggerate the negative effect of OA on coral calcification.

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