In recent decades, the marine environment has been seriously affected by various anthropogenic activities (e.g., deforestation, fossil fuel combustion, and disordered discharges of pollutants). As a consequence, a range of changes in seawater environmental factors have taken place in oceans around the world, including increased temperature, reduced pH and dissolved oxygen, salinity fluctuation, and many other anomalous alterations in environmental factors, and these changes have aroused concerns from scientists. It has been widely reported that these changes in environmental factors would impact marine organisms severely. Meanwhile, it is worth noting that the environmental stressors mentioned above are rarely occurring independently in nature. Thus marine organisms are usually threatened by many different environmental stressors, and there would be complex and unpredicted interactions among the stressors. Generally, the interactive effects varied among additive (total effect equal to the sum of individual effects), synergistic (total effect greater than the sum of individual effects), or antagonistic (total effect less than the sum of individual effects), depending on the species and life stages of the studied organism, and the nature of the stressors themselves. It is necessary to figure out the interactive effects among various environmental stressors on specific marine organisms to accurately predict their physiological states and population dynamics under future climate scenarios. Therefore in this chapter, we summarize the related experiments in the last 20 years to discuss the interactive effects of ocean acidification (OA) combined with four other typical environmental stressors, namely ocean warming, hypoxia, salinity fluctuation, and heavy metal pollution, on marine organisms according to previously published studies. The authors hope that the contents of this chapter provide some basic information about the interactive effects of OA and the other four environmental factors for readers who are interested in this subject area.
Uno de los factores que más influye las características químicas de un metal en solución es el nivel de acidez. El pH por lo tanto, afecta la reactividad del ion y por ende, su interacción con los puntos de unión de la pared celular de la planta. Este estudio evaluó el efecto del pH en la capacidad de bioacumulación de metales pesados en el alga roja Bostrychia calliptera (Rhodophyta, Rhodomelaceae), expuesta a diferentes rangos de pH. Se sometieron talos del alga a diferentes concentraciones de mercurio (Hg) y Plomo (Pb) a concentraciones desde: 0,1 hasta 10 mg l-1, para Hg y desde 0,1 hasta 15 mg l-1 para Pb, durante periodos exposición de 0, 12, 24 y 96 horas para cada ion, bajo diferentes niveles de pH. Las concentraciones de metal fueron determinadas por espectrofotometría de absorción atómica de acuerdo a los métodos estándar APHA. Las mayores tasas de acumulación se encontraron cuando el alga estaba expuesta a pH 7.8 (tanto para Hg como para Pb) el cual es un nivel de pH muy cercano al medido en el área de estudio. La concentración de metal en el alga se incrementó de manera lineal hasta las 48 hrs, tiempo donde se evidenció una mayor eficiencia de acumulación durante el primer intervalo del periodo del bioensayo.
- Effects of Cu2+ and elevated atmospheric CO2 on young sporophytes of Sargassum fusiforme were investigated.
- At elevated CO2, growth inhibition and pigment damage caused by Cu2+ remain at the same level.
- Elevated CO2 alleviates the Cu-induced suppression on photosystem.
- Elevated CO2 down-regulates the enzymatic antioxidant system against Cu2+.
Little attention has been given to the combined effects of elevated atmospheric CO2-induced ocean acidification (OA) and heavy metal pollution on marine macroalgae at the young stage. This study investigated the mutual effects of copper (Cu) and elevated CO2 on the young sporophytes of brown macroalgae Sargassum fusiforme. A matrix of four copper concentrations, 0, 0.025, 0.075 and 0.15 mg‧L-1, and two levels of CO2 (ambient CO2: 400 μatm; elevated CO2: 1,000 μatm) were used. High concentration of copper exposure greatly depressed photosynthesis and growth of the young sporophytes of S. fusiforme by reducing the apparent photosynthetic efficiency (ɑ), maximum net photosynthetic oxygen evolution rate (Pmax), maximum photochemical quantum yield (Fv/Fm) and pigments content (Chl a and Car). While elevated CO2 alone had obscure impact on this alga. However, the inhibition of Cu stress on Fv/Fm was weakened by elevated CO2, which also decreased the light compensation point (Ic). Meanwhile, the Cu2+-induced ascent in the dark respiration rate (Rd) and superoxide dismutase (SOD) activity was mitigated under the growth with elevated CO2, suggesting an alleviated oxidative stress. Overall, we propose that, under CO2 enrichment condition, the young sporophytes of S. fusiforme may increase photosynthesis efficiency and synthesize less enzymatic antioxidants in face of increasing Cu stress.
• Seasonal effects of Cd, warming and acidification on mussels target genes were assessed.
• mt-20 showed higher responsiveness to Cd exposure in digestive gland than in gills.
• hsp70 was sensitive to acidification in summer in digestive gland and in winter in gills.
• Cu/Zn-sod, gst-pi and cat showed tissue- and season-specific responses.
•Differences between tissues and seasons of investigation were demonstrated to occur.
Anthropogenic inputs of carbon dioxide in the atmosphere are driving ocean warming and acidification. The potential threat represented by these changes for marine species could be amplified in coastal areas, characterized by higher levels of pollutants. In addition, temperate organisms may exhibit a different seasonal tolerance to stressors influenced by fluctuations of environmental and physiological factors. In this study, Mediterranean mussels Mytilus galloprovincialis collected both in summer and winter were exposed to combinations of two temperatures (SST, seasonal surface temperature and SST+5 °C) and two levels of pH (8.20 and 7.40) in clean or cadmium contaminated seawater (20 μg/L Cd). mRNA levels of genes related to metal-induced stress response were investigated, including metallothionein mt-20, heat-shock protein hsp70, superoxide dismutase Cu/Zn-sod, catalase cat, glutathione peroxidase gpx1 and glutathione S-transferase gst-pi. To further elucidate if tissues with different physiological roles could exhibit different responsiveness, such analyses were carried out in digestive gland and in gills of exposed mussels. mt-20 mRNA increase after Cd-exposure was higher in the digestive gland than in the gills, with few modulations by temperature or pH only in the latter. Acidification, alone or in combination with other stressors, increased hsp70 mRNA, with seasonal- and tissue-specificities (higher in summer and in digestive gland). Among antioxidants, gpx1 mRNA was affected by Cd in both tissues and seasons, with further modulations due to pH and temperature variation tissue- and season-specific; in winter the combination of Cd, warming and acidification affected Cu/Zn-sod both in digestive gland and gills and cat only in gills, while weak seasonal variations were observed for gst-pi transcripts only in digestive gland. The overall results highlighted the importance of considering seasonality and responsiveness of different tissues to predict the effects of sudden changes in environmental parameters on responsiveness to and toxicity of chemicals in marine coastal organisms.
• Fluctuating pCO2/pH doubled copper-induced antioxidant activity and DNA damage in mussels.
• In contrast, fluctuating conditions mitigated some of the effects of copper for ragworms.
• These effects were associated with the differing acid-base physiology of the two species.
• Physiology was as important as changing copper chemistry in determining overall toxicity.
Global ocean pCO2 is increasing as a result of anthropogenic CO2 emissions, driving a decline in seawater pH. However, coastal waters already undergo fluctuations in pCO2/pH conditions over far shorter timescales, with values regularly exceeding those predicted for the open ocean by the year 2100. The speciation of copper, and therefore its potential toxicity, is affected by changing seawater pH, yet little is known concerning how present-day natural fluctuations in seawater pH affect copper toxicity to marine biota. Here, we test the hypothesis that a fluctuating seawater pCO2/pH regime will alter the responses of the mussel Mytilus edulis and the ragworm Alitta virens to sub-lethal copper, compared to a static seawater pCO2/pH scenario. Mussels and worms were exposed to 0.1 and 0.25 μM copper respectively, concentrations determined to produce comparable toxicity responses in these species, for two weeks under a fluctuating 12-hour pCO2/pH cycle (pH 8.14–7.53, pCO2 445–1747 μatm) or a static pH 8.14 (pCO2 432 μatm) treatment. Mussels underwent a haemolymph acidosis of 0.1–0.2 pH units in the fluctuating treatments, alongside two-fold increases in the superoxide dismutase activity and DNA damage induced by copper, compared to those induced by copper under static pH conditions. Conversely, ragworms experienced an alkalosis of 0.3 pH units under fluctuating pH/pCO2, driven by a two-fold increase in coelomic fluid bicarbonate. This mitigated the copper-induced oxidative stress to slightly reduce both antioxidant activity and DNA damage, relative to the static pH + copper treatment. These opposing responses suggest that differences in species acid-base physiology were more important in determining toxicity responses than the pH-induced speciation change. With variability in seawater chemistry predicted to increase as climate change progresses, understanding how fluctuating conditions interact with the toxicity of pH-sensitive contaminants will become more crucial in predicting their risk to coastal biota.
For coastal aquatic habitats the change in seawater pH occurring as a result of ocean acidification has the potential to alter the speciation and toxicity of the many contaminants that remain in high concentrations in coastal systems. Of particular concern are metals, such as copper, whose speciation is pH sensitive within the OA range. A meta-analysis of studies to date investigating OA-contaminant interactions using marine invertebrates reveals that 72% of the 44 studies conducted have indeed focused on metals such as copper, with only a few studies looking at polycyclic aromatic hydrocarbons (PAH) and pharmaceuticals. No clear trends in the pH-effect size on contaminant toxicity for either species or contaminant group were present however, suggesting species specific physiological responses may influence this interaction as well as contaminant chemistry. A relatively understudied group were the polychaetes, a key functional group for many coastal sediments. Sediments act as a sink for contaminants where they can accumulate to high concentrations. Hence there is high potential for polychaetes to experience elevated metal exposures under reduced seawater pH as OA progresses. To address this knowledge gap, the responses of two common coastal polychaete, Alitta virens and Hediste diversicolor, were studied under three different experimental scenarios (both water-borne and sediment based) focusing on the physiological and toxicological responses under combined exposures to ocean acidification and copper. Water-borne exposures of Alitta virens to 0.25 μM copper under ambient seawater (pH 8.10) showed a significant increase in DNA damage, along with a rise in both SOD activity and lipid peroxidation. However, when exposed to copper under OA conditions (pH 7.70) there was no further increase in DNA damage and a significant decrease in SOD activity was observed alongside a fall in lipid peroxidation suggesting that OA looks to buffer the toxicity responses to this species. This is in contrast to previous studies using mussels and sea urchins, where copper toxicity responses were significantly higher when exposed under OA conditions. To assess whether local adaptations to high levels of copper contamination influences this OA-copper interaction, a population comparison using a metal resistance population of the harbour ragworm, Hediste diversicolor and a nearby non-resistant population was then conducted. Exposures were run using copper concentrations that elicit comparable toxicity responses, using 0.50 uM copper for the resistant population, compared to 0.25 uM for the non-resistant population, reflecting the two-fold differences in LC50 values for these population. These experiments reveal a significant increase by 19.70% in metabolic rate effect size (the combined stressor when compared to the control) in the resistant population compared to a decrease by 24.02% the non-resistant population, along with differences in ammonia excretion rate and the O:N ratio, thus revealing an energetic cost of this genetic resistance when faced with the combined stressors of OA and copper. These data are in line with the emerging energy limited tolerance to stressors’ hypothesis which states that tolerance to stress can be energy limited, with bioenergetics playing a central role in the tolerance to environmental stress. Finally, a more environmentally realistic exposure scenario was conducted using Alitta virens to test the influence of sediment and tidal cycles on worm acid-base and oxidative stress responses. Field measurements of sediment pH revealed that the pHNBS range over a tidal cycle varies from 6.97 to 7.87, indicating that polychaetes are already experiencing pH’s lower than the predictions for near future open oceans. In aquarium exposures, with overlying water of pHNBS 8.10, sediment pHNBS remained within the range of 7.45 to 7.31, when the overlying water was manipulated to OA conditions (pHNBS 7.70) sediment pHNBS was within the same range as the ambient treatment. The lack of change in sediment pH, despite a 0.40 unit drop in seawater pH, removed any comparative differences in physiological and toxicity end points in the worms between treatments. Tidal emersion induced a slight reduction in sediment pH, with a significant copper effect on sediment pH causing a further decrease in pH levels. Interestingly emersion resulted in a significant OA-copper interaction for coelomic fluid bicarbonate, which increased over the emersion period, however, there was no emersion driven acidosis within coelomic fluid. Overall this work further points to contaminant-OA interactions being species specific driven, in part driven by animal physiology. It also highlights the importance of environmentally relevant exposures with sediment dwelling organisms experiencing lower pH levels than the overlying seawater which could potentially affect metal speciation and could lead to OA-contaminant interactions occurring very differently in this environment. These are important considerations for ecotoxicology studies in the face of global ocean changes.
Ocean acidification (OA) is usually thought to change the speciation of trace metals and increase the concentration of free metal ions, hence elevating metal bioavailability. In this study, embryos of the oyster Crassostrea angulata and abalone Haliotis discus hannai were cultured under 4 pCO2 conditions (400, 800, 1500 and 2000 µatm) with Cu and Zn added. Fertilization rate was measured 2 h post-fertilization (hpf), while larval deformation and larval shell length were measured 24 hpf. Our results show that OA can alleviate Cu and Zn inhibition of C. angulata fertilization by 86.1 and 26.4% respectively, and Zn inhibition of H. discus hannai fertilization by 43.7%. However, OA enhanced the inhibitory effect of Cu on fertilization of H. discus hannai by 34.7%. OA enhanced the toxic effect of Cu on larval normality of C. angulata by 22.0% and the effect of Cu and Zn on larval normality of H. discus hannai by 71.4 and 37.2%, respectively. OA also enhanced the inhibitory effects of Cu and Zn on larval calcification in H. discus hannai by 8.8 and 8.6%, respectively. However, OA did not change the effect of Cu on the calcification of C. angulata larvae. OA decreased Zn inhibition of oyster larval calcification from 3.1 to 1.5%. Based on our results, the toxic effects of metal on early development of molluscs are not always increased by rising pCO2 and differ across developmental stages, egg structure and species. This complexity suggests that caution should be taken when carrying out multiple environmental stressor tests on molluscan embryos.
Changes in seawater pH can alter the chemical speciation of waterborne chemical elements, affecting their bioavailability and, consequently, their bioaccumulation in marine organisms. Here, controlled environmental conditions and a 210Pb radiotracer were used to assess the effect of five distinct pH conditions (pHT ranging from 7.16 to 7.94) on the short-term (9 days) accumulation of Pb in the blue mussel, Mytilus edulis. After 9 days of exposure, higher levels of Pb were observed in the soft tissues of mussels maintained in the lower pH conditions, while Pb levels accumulated by mussel shells showed no difference across pH conditions. These results suggest that pH decreases such as those predicted by ocean acidification scenarios could enhance Pb contamination in marine organisms, with potential subsequent contamination and effect risks for human consumers.
Mercury (Hg) is globally recognized as a persistent chemical contaminant that accumulates in marine biota, thus constituting an ecological hazard, as well as a health risk to seafood consumers. Climate change-related stressors may influence the bioaccumulation, detoxification, and toxicity of chemical contaminants, such as Hg. Yet, the potential interactions between environmental stressors and contaminants, as well as their impacts on marine organisms and seafood safety, are still unclear. Hence, the aim of this work was to assess the bioaccumulation of Hg and neuro-oxidative responses on the commercial flat fish species Solea senegalensis (muscle, liver, and brain) co-exposed to dietary Hg in its most toxic form (i.e., MeHg), seawater warming (ΔT°C = +4 °C), and acidification (pCO2 = +1000 µatm, equivalent to ΔpH = −0.4 units). In general, fish liver exhibited the highest Hg concentration, followed by brain and muscle. Warming enhanced Hg bioaccumulation, whereas acidification decreased this element’s levels. Neuro-oxidative responses to stressors were affected by both climate change-related stressors and Hg dietary exposure. Hazard quotient (HQ) estimations evidenced that human exposure to Hg through the consumption of fish species may be aggravated in tomorrow’s ocean, thus raising concerns from the seafood safety perspective.
Brown seaweed, Padina boryana is found along the coast of Terengganu, Malaysia and may serve as a potential heavy metal biomonitor in the coastal zones. To better understand the impact of heavy metal pollution on P. boryana at varying seawater pH levels, the combined effect of zinc (Zn) and pH on its growth rate and chlorophyll content was investigated in laboratory exposures. After exposure for 21 days in a mixed treatment of 6 pH variations (4 to 9) and three Zn concentrations (30, 150, 300 ppb), maximum growth rate was observed in controlled treatments at pH 8 with no added Zn, whereas treatments at pH 4 and 9 showed negative growth rates after 18 days. The growth rate and chlorophyll content of P. boryana decreased significantly with an increase in Zn concentration. At pH 6, 7 and 8, P. boryana showed significant decreases (p < 0.05) in growth rates and chlorophyll content in all concentrations of Zn compared with control plants (no Zn). At pH of 6.0 and below, controls were also affected with significantly reduced growth rates and chlorophyll contents while Zn treated seaweed showed significant effects compared to these controls. The effect of pH and Zn on all measured factors was obvious on Day 6 onwards, whereas the interaction effect between them was significant on chlorophyll content throughout the experiment. From Day 9 onwards, the growth rate and chlorophyll content showed significant correlation among each other.
Rising concentrations of atmospheric carbon dioxide are causing ocean acidification and will influence marine processes and trace metal biogeochemistry. In June 2012, in the Raunefjord (Bergen, Norway), we performed a mesocosm experiment, comprised of a fully factorial design of ambient and elevated pCO2 and/or an addition of the siderophore desferrioxamine B (DFB). In addition, the macronutrient concentrations were manipulated to enhance a bloom of the coccolithophore Emiliania huxleyi. We report the changes in particulate trace metal concentrations during this experiment. Our results show that particulate Ti and Fe were dominated by lithogenic material, while particulate Cu, Co, Mn, Zn, Mo and Cd had a strong biogenic component. Furthermore, significant correlations were found between particulate concentrations of Cu, Co, Zn, Cd, Mn, Mo and P in seawater and phytoplankton biomass (µgC L−1), supporting a significant influence of the bloom in the distribution of these particulate elements. The concentrations of these biogenic metals in the E. huxleyi bloom were ranked as follows: Zn < Cu ≈ Mn < Mo < Co < Cd. Changes in CO2 affected total particulate concentrations and biogenic metal ratios (Me : P) for some metals, while the addition of DFB only significantly affected the concentrations of some particulate metals (mol L−1). Variations in CO2 had the most clear and significant effect on particulate Fe concentrations, decreasing its concentration under high CO2. Indeed, high CO2 and/or DFB promoted the dissolution of particulate Fe, and the presence of this siderophore helped in maintaining high dissolved Fe. This shift between particulate and dissolved Fe concentrations in the presence of DFB, promoted a massive bloom of E. huxleyi in the treatments with ambient CO2. Furthermore, high CO2 decreased the Me : P ratios of Co, Zn and Mn while increasing the Cu : P ratios. These findings support theoretical predictions that the molar ratios of metal to phosphorous (Me : P ratios) of metals whose seawater dissolved speciation is dominated by free ions (e.g., Co, Zn and Mn) will likely decrease or stay constant under ocean acidification. In contrast, high CO2 is predicted to shift the speciation of dissolved metals associated with carbonates such as Cu, increasing their bioavailability and resulting in higher Me : P ratios.
• Seawater acidification and Cd induced oxidative stress in flounder larvae.
• Two stressors interacted to regulate mRNA expressions of antioxidant-related genes.
• Integrated antioxidant response was promoted with increasing oxidative stress.
Increasing atmospheric carbon dioxide has led to a decrease in the pH of the ocean, which influences the speciation of heavy metals and consequently affects metal toxicity in marine organisms. To investigate the effects of seawater acidification and metals on the antioxidant defenses of marine fishes, the flounder Paralichthys olivaceus, was continuously exposed to cadmium (Cd; control, 0.01 and 0.15 mg L−1) and acidified seawater (control (pH 8.10), 7.70 and 7.30) for 49 days from embryogenesis to settlement. The results demonstrated that both Cd and acidified seawater could induce oxidative stress and consequently cause lipid peroxidation (LPO) in the larvae. Antioxidants (i.e., superoxide dismutase, SOD; catalase, CAT; reduced glutathione, GSH; glutathione S-transferase, GST; glutathione peroxidase, GPx; and glutathione reductase, GR) functioned to defend the larvae against oxidative damage. Overall, Cd induced (SOD, GST and GSH) or inhibited (CAT and GPx) the enzymatic activities or contents of all the selected antioxidants except for GR. The antioxidants responded differently to seawater acidification, depending on their interaction with the metal. Similarly, the mRNA expressions of the antioxidant-related genes were upregulated (sod, gr and gst) or downregulated (cat and gpx) in response to increasing Cd exposure. Seawater acidification did not necessarily affect all of the biomarkers; in some cases (e.g., SOD and sod, GR and gr), Cd stress may have exceeded and masked the stress from seawater acidification in regulating the antioxidant defense of the larvae. The integrated biomarker response (IBR) was enhanced with increasing levels of the stressors. These findings support the hypothesis that seawater acidification not only directly affects the antioxidant defense in flounder larvae but also interacts with Cd to further regulate this defense. This study has ecological significance for assessing the long-term impacts of ocean acidification and metal pollution on the recruitment of fish populations in the wild.
• Phytoplankton showed higher resilience to increasing CO2.
• Few centric diatoms showed positive response to increasing CO2 supply.
• Addition of Zn under increasing CO2 inhibited cell division, but not biomass.
• The combined effects of increasing CO2 and Cu addition was insignificant on growth.
• Cu addition at high CO2 level promoted toxigenic pennate diatom growth.
Increasing dissolution of CO2 in the surface ocean is rapidly decreasing its pH and changing carbon chemistry which is further affecting marine biota in several ways. Phytoplankton response studies under the combination of elevated CO2 and trace metals are rare. We have conducted two consecutive onboard incubation experiments (R. V. Sindhu Sadhana; August 2017) in the eastern Arabian Sea (SW coast of India) during an upwelling event. A nutrient enriched diatom bloom was initiated onboard and grown under ambient (≈400 μatm, A-CO2) and high CO2 levels (≈1000 μatm; H–CO2) with different zinc (Zn; 1 nM) and copper (Cu) concentrations (1 nM, 2 nM and 8 nM). Phytoplankton community composition and the dominant genera were different during these two experiments. CO2 enrichment alone did not show any significant growth stimulating impact on the experimental community except enhanced cell density in the first experiment. Addition of Zn at A-CO2 level revealed no noticeable responses; whereas, the same treatment under H–CO2 level significantly reduced cell number. Considerably high protein content under H–CO2+Zn treatment was possibly counteracting Zn toxicity which also caused slower growth rate. Cu addition did not show any noticeable impact on growth and biomass production except increased protein content as well as decreased carbohydrate: protein ratio. This can be attributed to relatively higher protein synthesis than carbohydrate to alleviate oxidative stress generated by Cu. The centric diatom Chaetoceros and toxin producing pennate diatom Pseudo-nitzschias howed no significant response to either CO2 or Zn enrichment. Large centric diatom Leptocylindrus and Skeletonema responded positively to Zn addition in both CO2 levels. The former species showed the most sensitive response at the highest Cu and H–CO2 treatment; whereas, the pennate diatoms Nitzschia and Pseudo-nitzschia (toxigenic diatom) showed higher resilience under elevated CO2 and Cu levels. This observation indicated that in future ocean, increasing CO2 concentrations and trace metal pollution may potentially alter phytoplankton community structure and may facilitate toxigenic diatom bloom in the coastal waters.
• OA significantly alleviated the toxicity of Cd to S. costatum.
• OA rescued S. costatum from inhibition of Cd on photosynthesis and pyruvate metabolism.
• OA detoxified Cd through upregulating genes in production of non-protein thiol compounds.
Ocean acidification (OA) is a global problem to marine ecosystems. Cadmium (Cd) is a typical metal pollutant, which is non-essential but extremely toxic to marine organisms. The combined effects of marine pollution and climate-driven ocean changes should be considered for the effective marine ecosystem management of coastal areas. Previous reports have separately investigated the influences of OA and Cd pollution on marine organisms. However, little is known of the potential combined effects of OA and Cd pollution on marine diatoms. We investigated the sole and combined influences of OA (1,500 ppm CO2) and Cd exposure (0.4 and 1.2 mg/L) on the coastal diatom Skeletonema costatum. Our results clearly showed that OA significantly alleviated the toxicity of Cd to S. costatum growth and mitigated the oxidant stress, although the intercellular Cd accumulation still increased. OA partially rescued S. costatum from the inhibition of photosynthesis and pyruvate metabolism caused by Cd exposure. It also upregulated genes involved in gluconeogenesis, glycolysis, the citrate cycle (TCA), Ribonucleic acid (RNA) metabolism, and especially the biosynthesis of non-protein thiol compounds. These changes might contribute to algal growth and Cd resistance. Overall, this study demonstrates that OA can alleviate Cd toxicity to S. costatum and explores the potential underlying mechanisms at both the cellular and molecular levels. These results will ultimately help us understand the impacts of combined stresses of climate change and metal pollution on marine organisms and expand the knowledge of the ecological risks of OA.
The globally changing environmental climate, ocean acidification, and heavy metal pollution are of increasing concern. However, studies investigating the combined effects of ocean acidification and zinc (Zn) exposure on macroalgae are very scarce. In this study, the photosynthetic performance of the red alga Pyropia yezoensis was examined under three different concentrations of Zn (control, 25 (medium), and 100 (high) μg L−1) and pCO2 (400 (ambient) and 1000 (high) μatm). The results showed that higher Zn concentrations resulted in increased toxicity for P. yezoensis, while ocean acidification alleviated this negative effect. Ocean acidification increased the relative growth rate of thalli under both medium and high Zn concentrations. The net photosynthetic rate and respiratory rate of thalli also significantly increased in response under ocean acidification, when thalli were cultured under both medium and high Zn concentrations. Malondialdehyde levels decreased under ocean acidification, compared to ambient CO2 conditions and either medium or high Zn concentrations. The activity of superoxide dismutase increased in response to high Zn concentrations, which was particularly apparent at high Zn concentration and ocean acidification. Immunoblotting tests showed that ocean acidification increased D1 removal, with increasing expression levels of the PSII reaction center proteins D2, CP47, and RbcL. These results suggested that ocean acidification could alleviate the damage caused by Zn exposure, thus providing a theoretical basis for a better prediction of the impact of global climate change and heavy metal contamination on marine primary productivity in the form of seaweeds.
Carbon nanomaterials (CNM), such as graphene oxide (GO), have been the focus of study in several areas of science mostly due to their physical-chemical properties. However, data concerning the potential toxic effects of these CNM in bivalves are still scarce. When present in the aquatic systems, the combination with other contaminants, as well as pH environmental variations, can influence the behavior of these nanomaterials and, consequently, their toxicity. Thus, the main goal of this study was to evaluate the effect of exposure of clam Ruditapes philippinarum to GO when acting alone and in the combination with copper (Cu), under two pH levels (control 7.8 and 7.3). A 28-day exposure was performed and metabolism and oxidative stress-related parameters were evaluated. The effects caused by GO and Cu exposures, either isolated or co-exposed, showed a direct and dependent relationship with the pH in which the organisms were exposed. In clams maintained at control pH (7.8), Cu and GO + Cu treatments showed lower lipid peroxidation (LPO) and lower electron transport system (ETS) activity, respectively. In clams maintained at low pH, glutathione-S-transferases (GSTs) activities were increased in Cu and Cu + GO treatments, whereas reduced glutathione (GSH) levels were increased in Cu treatment and ETS activity was higher in GO + Cu. Thus, it can be observed that clams responses to Cu and GO were strongly modulated by pH in terms of their defense system and energy production, although this does not result into higher LPO levels.
• Combined effects of OA and Cd exposure on Phaeodactylum tricornutum were analyzed.
• Either OA (1500 ppm) or Cd stress (1.2 mg/L) alone inhibited the growth of P. tricornutum.
• A significantly enhanced tolerance of P. tricornutum to Cd of 1.2 mg/L occurred under OA.
Ocean acidification (OA) and heavy metals are common stress factors for marine ecosystems subject to anthropogenic impacts. OA coupled with the heavy metal is likely to affect marine species. This study investigated the single and combined effects of OA (1500 ppm) and cadmium (Cd; 0.4, 1.2 mg/L) on the marine diatom Phaeodactylum tricornutum under 7 d exposure. The results clearly indicated that either OA or Cd stress (1.2 mg/L) alone inhibited the growth of P. tricornutum. However, under the combined OA-Cd stress, the growth inhibition disappeared, and the intracellular oxidative damage was mitigated. These results indicated a significantly enhanced tolerance of P. tricornutum to Cd while under OA conditions, which could be beneficial to the survival of this diatom. This study will ultimately help us understand the responses of marine organisms to multiple stressors and have broad implications for the potential ecological risks of Cd under future OA conditions.
• Copper increased bleaching, respiration and inhibited calcification-related enzymes.
• Thermal stress was the main driver of mortality.
• Relative tolerance to climate change scenario (ocean warming + acidification).
• Integrated biomarker response related more to co-exposures than isolated biomarkers.
• Integrated analysis showed higher stress under climate change + copper condition.
Multiple global and local stressors threat coral reefs worldwide, and symbiont-bearing foraminifera are bioindicators of reef health. The aim of this study was to investigate single and combined effects of copper (Cu) and climate change related stressors (ocean acidification and warming) on a symbiont-bearing foraminifer by means of an integrated biomarker analysis. Using a mesocosm approach, Amphistegina gibbosa were exposed for 25 days to acidification, warming and/or Cu contamination on a full orthogonal design (two levels each factor). Cu was the main factor increasing bleaching and respiration rates. Warming was the main cause of mortality and reduced growth. Calcification related enzymes were inhibited in response to Cu exposure and, in general, the inhibition was stronger under climate change. Multiple biological endpoints responded to realistic exposure scenarios in different ways, but evidenced general stress posed by climate change combined with Cu. These biological responses drove the high values found for the ‘stress index’ IBR (Integrated Biomarker Response) – indicating general organismal health impairment under the multiple stressor scenario. Our results provide insights for coral reef management by detecting potential monitoring tools. The ecotoxicological responses indicated that Cu reduces the tolerance of foraminifera to climate change (acidification + warming). Once the endpoints analysed have a high ecological relevance, and that responses were evaluated on a classical reef bioindicator species, these results highlight the high risk of climate change and metal pollution co-exposure to coral reefs. Integrated responses allowed a better effects comprehension and are pointed as a promising tool to monitor pollution effects on a changing ocean.
Previous work with isolated outer membrane vesicles of lobster branchiostegite epithelial cells has shown that 45Ca2+ uptake by these structures is significantly (p < 0.02) reduced by an incremental decrease in saline pH (increased proton concentration) and that this decrease is due to competitive inhibition between carrier-mediated transport of 45Ca2+ and hydrogen ions. The present paper extends these previous findings and describes the combined effects of pH and cationic heavy metals on branchiostegite uptake of 45Ca2+. Partially purified membrane vesicles of branchiostegite cells were produced by a homogenization/centrifugation method and were loaded with mannitol at pH 7.0. The time course of 1 mM 45Ca2+ uptake in a mannitol medium at pH 8.5 containing 100 µM verapamil (Ca2+ channel blocker) was hyperbolic and approached equilibrium at 30 min. This uptake was either significantly reduced (p < 0.05) by the addition of 5 µM Zn2+ or essentially abolished with the addition of 5 µM Cu2+. Increasing zinc concentrations (5–500 µM) reduced 1 mM 45Ca2+ uptake at pH 8.5 or 7.5 in a hyperbolic fashion with the remaining non-inhibited uptake due to apparent non-specific binding. Uptake of 1 mM 45Ca2+ at pH 8.5, 7.5, 7.5 + Zn2+, and 7.5 + Zn2+ + Cu2+ + Cd2+ in the presence of 100 µM verapamil displayed a stepwise reduction of 45Ca2+ uptake with the addition of each treatment until only non-specific isotope binding occurred with all cation inhibitors. 45Ca2+ influxes (15 s uptakes; 0.25–5.0 mM calcium + 100 µM verapamil) in the presence and absence of 10 µM Zn2+ were both hyperbolic functions of calcium concentration. The curve with Zn2+ displayed a transport Km twice that of the control (p < 0.05), while inhibitor and control curve Jmax values were not significantly different (p > 0.05), suggesting competitive inhibition between 45Ca2+ and Zn2+ influxes. Analysis of the relative inhibitory effects of increased proton or heavy metal interaction with 45Ca2+ uptake suggests that divalent metals may reduce the calcium transport about twice as much as a drop in pH, but together, they appear to abolish carrier-mediated transport.