Globally, kelp forests are threatened by multiple stressors, including increasing grazing by sea urchins. With coastal upwelling predicted to increase in intensity and duration in the future, understanding whether kelp forest and urchin barren urchins are differentially affected by upwelling-related stressors will give insight into how future conditions may affect the transition between kelp forests and barrens. We assessed how current and future-predicted changes in the duration and magnitude of upwelling-associated stressors (low pH, dissolved oxygen, and temperature) affected the performance of purple sea urchins (Strongylocentrotus purpuratus) sourced from rapidly-declining bull kelp (Nereocystis leutkeana) forests and nearby barrens and maintained on habitat-specific diets. Kelp forest urchins were of superior condition to barrens urchins, with ~ 6–9 times more gonad per body mass. Grazing and condition in kelp forest urchins were more negatively affected by distant-future and extreme upwelling conditions, whereas grazing and survival in urchins from barrens were sensitive to both current-day and all future-predicted upwelling, and to increases in acidity, hypoxia, and temperature regardless of upwelling. We conclude that urchin barren urchins are more susceptible to increases in the magnitude and duration of upwelling-related stressors than kelp forest urchins. These findings have important implications for urchin population dynamics and their interaction with kelp.
This study investigated the combined effects of seawater acidification and hypoxia on the antioxidant response in gonads of the thick shell mussel Mytilus coruscus. Mussels were collected along the Shengsi Island, East China Sea, where oxygen and pH fluctuations frequently occur in summer. Mussels were exposed to three pH (8.1, 7.7, and 7.3) and two dissolved oxygen (DO) levels (6 and 2 mg L−1) for 21 days followed by a 10-day recovery period (pH 8.1 and DO 6 mg L-1). Gonad surface area (GSA) and activity of superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPX), glutathione (GSH), glutathione S-transferase (GST), and malondialdehyde (MDA) in gonad were measured at days 21 and 31. Complex and enzyme-specific responses were observed after the 21-day exposure period. Overall, PCA analysis revealed a stronger effect of pH than DO. Integrated biomarker response (IBR) analysis demonstrated that low pH and DO decreased mussel’s antioxidant system and increased oxidative damage with potential consequences for gonad development. Mussels exposed to low pH and DO were only partly able to recover a normal enzymatic activity after 10-day recovery period. This suggests that mussels exposed to short-term pH and DO fluctuations event in the field may suffer lasting negative impacts.
Ocean chemistry is changing as a result of human activities. Atmospheric carbon dioxide (CO2) concentrations are increasing, causing an increase in oceanic pCO2 that drives a decrease in oceanic pH, a process called ocean acidification (OA). Higher CO2 concentrations are also linked to rising global temperatures that can result in more stratified surface waters, reducing the exchange between surface and deep waters; this stronger stratification, along with nutrient pollution, contributes to an expansion of oxygen-depleted zones (so called hypoxia or deoxygenation). Determining the response of marine organisms to environmental changes is important for assessments of future ecosystem functioning. While many studies have assessed the impact of individual or paired stressors, fewer studies have assessed the combined impact of pCO2, O2, and temperature. A long-term experiment (∼10 months) with different treatments of these three stressors was conducted to determine their sole or combined impact on the abundance and survival of a benthic foraminiferal community collected from a continental-shelf site. Foraminifera are well suited to such study because of their small size, relatively rapid growth, varied mineralogies and physiologies. Inoculation materials were collected from a ∼77-m deep site south of Woods Hole, MA. Very fine sediments (<53 μm) were used as inoculum, to allow the entire community to respond. Thirty-eight morphologically identified taxa grew during the experiment. Multivariate statistical analysis indicates that hypoxia was the major driving factor distinguishing the yields, while warming was secondary. Species responses were not consistent, with different species being most abundant in different treatments. Some taxa grew in all of the triple-stressor samples. Results from the experiment suggest that foraminiferal species’ responses will vary considerably, with some being negatively impacted by predicted environmental changes, while other taxa will tolerate, and perhaps even benefit, from deoxygenation, warming and OA.
- Ocean acidification adversely affects the gonadal performance of mussels.
- Hypoxia does not have effects on fecundity of mussels.
- Steroids and Wnt/β-catenin gene expressions have weak correlations with fecundity in mussels.
Ocean acidification and hypoxia have become increasingly severe in coastal areas, and their co-occurrence poses emerging threats to coastal ecosystems. Here, we investigated the combined effects of ocean acidification and hypoxia on the reproductive capacity of the thick-shelled mussel Mytilus coruscus. Our results demonstrated low pH but not low oxygen induced decreased gonadosomatic index (GSI) in mussels. Male mussels had a lower level of sex steroids (estradiol, testosterone, and progesterone) when kept at low pH. Expression of genes related to reproduction were also impacted by low pH with a downregulation of genes involved in gonad development in males (β-catenin and Wnt-7b involved in males) and an upregulation of testosterone synthesis inhibition-related gene (Wnt-4) in females. Overall, our results suggest that ocean acidification has an impact on the gonadal development through an alternation of gene expression and level of steroids while hypoxia had no significant effect.
Krill are abundant and ecologically important zooplankton that inhabit dynamic environments characterized by strong natural variability, but global ocean change is shifting the range of conditions that they experience. Laboratory tests reveal that krill are sensitive to ocean acidification despite residing in naturally low pH areas, showing the importance of modulating factors for determining their responses. This study combines laboratory manipulations with field observations across a strong natural water chemistry gradient in Puget Sound, Washington, USA to investigate the effects of pH and oxygen on adult female North Pacific krill, Euphausia pacifica. Enzyme activities of the Electron Transport System (ETS) and aminoacyl-tRNA synthetases (AARS) were used as indices of zooplankton metabolism and growth, respectively, and were paired with traditional incubation methods. Acclimation to pH and oxygen conditions in the laboratory did not reveal effects on respiration rate, ETS, or AARS activity of krill. However, field observations showed that respiratory potential, as estimated by ETS activity, decreased with decreasing oxygen, declining 9% (95% confidence interval 2.5–15%) over the range of conditions we observed (3.9–8.1 mg O2 L−1). This reduction would depress the metabolic potential of krill in areas of stressful conditions (concurrent low pH), though krill also displayed a high degree of inter-individual variability. Although differences in age structure suggest different patterns of recruitment between E. pacifica populations in areas with stressful conditions and those without, populations persist at stressful sites. Lower temperature of waters with low oxygen and pH, as well as high food concentrations, may contribute to these populations’ success.
Global climate change is driving shifts in ocean chemistry, which combined with intensification of coastal upwelling, reduces ocean pH and dissolved oxygen (DO) content in the nearshore habitats of the California Current System. Physiological plasticity, within and across generations, might be especially important for long-lived, late-to-mature species, like rockfishes (genus Sebastes), that may be unable to keep pace with climate change via genetic adaptation. Rockfishes exhibit matrotrophic viviparity and may be able to buffer their offspring from environmental stress through early developmental exposure or transgenerational plasticity (non-genetic inheritance of phenotypes). In this study, mature female gopher (S. carnatus) and blue (S. mystinus) rockfish were pre-exposed to one of four treatments; 1) control conditions, 2) low pH, 3) low DO, or 4) combined low pH/DO stressors during embryonic growth (i.e. fertilization and gestation), followed by a 5-day larval exposure after birth in either the same or a different treatment received by mothers. I used RNA sequencing to determine how the maternal environment affected larval rockfish gene expression (GE) at birth, after the 5-day larval exposure in either the same maternal treatment or a novel pH/DO environment, and between larvae sampled at birth and after the 5-day larval exposure within each treatment. For both species, I found that the maternal exposure drove larval GE patterns regardless of sampling time point or treatment. Furthermore, the maternal environment continued to strongly influence larval GE for at least the first five days after birth. In gopher rockfish, larvae differentially expressed fewer genes at birth between the control and hypoxic groups than larvae that gestated in and remained in the same treatment and were sampled after the 5-day larval exposure. Gene functions also shifted; at day 5, there was an increase in differentially expressed genes that were related to metabolic pathways, implying that the larvae in the hypoxic treatment are responding to the stressor. In both species, I found that larvae which experienced a pH and/or hypoxic stressor during the maternal exposure had fewer differentially expressed genes across time compared to larvae that experienced control conditions. This pattern remained consistent, even if the larvae were placed into control conditions for the 5-day larval exposure, indicating that exposure to low pH/DO stressors might cause a delay in development. These data suggest that rockfish may not be able to buffer their offspring from environmental stressors, highlighting the important role of the maternal environment during gestation. Between the two species, however, blue rockfish may in fact fare better in future conditions as their reproductive season occurs before the onset of strong spring upwelling, when more hypoxic and low pH water intrudes the nearshore. However, if future climate models are correct, shifts in the timing and intensity of upwelling season may overlap with the reproductive season in blue rockfish. Elucidating the critical role of the maternal environment on offspring physiology can help us better understand how economically and ecologically important species will fare in the face of climate change.
Global change has resulted in oceans that are warmer, more acidic, and lower in oxygen. Individually any one of these stressors can have numerous negative impacts on marine organisms, and in combination they are likely to be particularly detrimental. Understanding the interactions between these factors is important as they often covary, with warming promoting hypoxia, and hypoxia co-occurring with acidification. Few studies have examined how all three factors interact to affect organismal performance, and information is particularly sparse for tropical organisms. Here we documented a strong relationship between high temperatures, low dissolved oxygen (DO), and low pH in and around a tropical bay. We used these field values to inform two multi-stressor experiments. Each experimental factor had two levels, one representing current average conditions and the other representing current extreme conditions experienced in the area. We used sea urchin righting response as a measure of organismal performance for an important reef herbivore. In the first experiment 2-h exposures to a fully factorial combination of temperature, DO, and pH showed that righting success was significantly depressed under low oxygen. To more fully understand the impacts of pH, we acclimated sea urchins to control and low pH for 7 days and subsequently exposed them to the same experimental conditions. Sea urchins acclimated to control pH had significantly reduced righting success compared to animals acclimated to low pH, and righting success was significantly depressed under hypoxia and high temperature, compared to normoxia and ambient temperature. These results show that short, 2 h exposures to the temperature and DO extremes that are already experienced periodically by these animals have measurable detrimental effects on their performance. The positive impact of reduced pH is evident only over longer, 7 days durations, which are not currently experienced in this area.
- Low pH, low DO and high temperature have adverse effects on the antioxidant parameters.
- Exposure time of stressors has significant effects on the antioxidant parameters.
- Combined stressors exert more severe effects on the antioxidant indicators than single ones.
In the present study, the combined effects of pH, dissolved oxygen (DO) and temperature levels on the antioxidant responses of the mussel Mytilus coruscus were evaluated. Mussels were exposed to two pH (8.1, 7.7-acidification), two DO (6 mg L−1, 2 mg L−1-hypoxia) and two temperature levels (20 °C, 30 °C-warming) for 30 days. SOD, CAT, MDA, GPx, GSH, GST, TAOC, AKP, ACP, GPT, AST levels were measured in the gills of mussels. All tested biochemical parameters were altered by these three environmental stressors. Values for all the test parameters except GSH first increased and then decreased at various experimental treatments during days 15 and 30 as a result of acidification, hypoxia and warming. GSH content always increased with decreased pH, decreased DO and increased temperature. PCA showed a positive correlation among all the measured biochemical indexes. IBR results showed that M. coruscus were adversely affected by reduced pH, low DO and elevated temperature.
Pacific salmon stocks are in decline with climate change named as a contributing factor. The North Pacific coast of British Columbia is characterized by strong temporal and spatial heterogeneity in ocean conditions with upwelling events elevating CO2 levels up to 10-fold those of pre-industrial global averages. Early life stages of pink salmon have been shown to be affected by these CO2 levels, and juveniles naturally migrate through regions of high CO2 during the energetically costly phase of smoltification. To investigate the physiological response of out-migrating wild juvenile pink salmon to these naturally occurring elevated CO2 levels, we captured fish in Georgia Strait, British Columbia and transported them to a marine lab (Hakai Institute, Quadra Island) where fish were exposed to one of three CO2 levels (850, 1500 and 2000 μatm CO2) for 2 weeks. At ½, 1 and 2 weeks of exposure, we measured their weight and length to calculate condition factor (Fulton’s K), as well as haematocrit and plasma [Cl−]. At each of these times, two additional stressors were imposed (hypoxia and temperature) to provide further insight into their physiological condition. Juvenile pink salmon were largely robust to elevated CO2 concentrations up to 2000 μatm CO2, with no mortality or change in condition factor over the 2-week exposure duration. After 1 week of exposure, temperature and hypoxia tolerance were significantly reduced in high CO2, an effect that did not persist to 2 weeks of exposure. Haematocrit was increased by 20% after 2 weeks in the CO2 treatments relative to the initial measurements, while plasma [Cl−] was not significantly different. Taken together, these data indicate that juvenile pink salmon are quite resilient to naturally occurring high CO2 levels during their ocean outmigration.
Among global coastal regions, the Northern California Current System (N-CCS) is already experiencing effects from ocean acidification and hypoxia during the summer, primarily due to the region’s seasonal upwelling, current systems, and high productivity. Oxygen, pH, and temperature conditions are expected to become more stressful with continued fossil fuel emissions under global climate change, posing a serious threat to the region’s fisheries. N-CCS fishing communities rely heavily on the economically and culturally important Dungeness crab (Metacarcinus magister). The fishery is currently sustainably managed, but potential negative impacts from changing ocean conditions on Dungeness crab life stages and populations could have adverse effects for the fishery and the communities that rely on it. To quantify the vulnerability of Dungeness crab life stages and populations to predicted future conditions, both model projections and empirical experiments need to be employed. A semi-quantitative, life stage-specific framework was adapted here to assess the vulnerability of Dungeness crab to low pH, low dissolved oxygen, and high temperature under present and future projected conditions in the seasonally dynamic N-CCS. This was achieved using a combination of regional ocean models, species distribution maps, larval transport models, a population matrix model, and a literature review. This multi-faceted approach revealed that crab vulnerability to the three climate stressors will increase in the future (year 2100) under the most intense emissions scenario, with vulnerability to low oxygen being the most severe to the N-CCS population overall. Increases in vulnerability were largely driven by the adult life stage, which contributes the most to population growth. Empirical experiments demonstrated that adult crab respiration rates increase exponentially with temperature, potentially making this life stage more susceptible to hypoxia in the future. Together, this work provides novel insights into the effects of changing ocean conditions on Dungeness crab populations, which may help inform fishery management strategies.
Normally atmospheric CO2 is the major driver of ocean acidification (OA); however, local discharge/degradation of organic matter (OM) and redox reactions can exacerbate OA in coastal areas. In this work we study the response of nutrient and carbon systems to pH decrease in relation to hydrographically induced intermittent characteristics and examine scenarios for future ocean acidification in a coastal system. Laboratory microcosm experiments were conducted using seawater and surface sediment collected from the deepest part of Elefsis Bay; the pH was constantly being monitored while CO2 gas addition was adjusted automatically. In Elefsis Bay surface pCO2 is already higher than global present atmospheric values, while near the bottom pCO2 reaches 1538 μatm and carbonate saturation states were calculated to be around 1.5. During the experiment, in more acidified conditions, limited alkalinity increase was observed and was correlated with the addition of bicarbonates and OM. Ammonium oxidation was decelerated and a nitrification mechanism was noticed, despite oxygen deficiency, paralleled by reduction of Mn-oxides. Phosphate was found significantly elevated for the first time in lower pH values, without reprecipitating after reoxygenation; this was linked with Fe(II) oxidation and Fe(III) reprecipitation without phosphate adsorption affecting both available dissolved phosphate and (dissolved inorganic nitrogen) DIN:DIP (dissolved inorganic phosphate)ratio.
•Combined occurrence of hypoxia, acidification and nutrients increased biofilm bacterial diversity and richness
•Elevated nutrients, and depleted oxygen and pH levels resulted in different bacterial community composition
•Higher abundance of Flavobacteriales, Epsilonproteobacteria and Vibrionales, but less Oceanospirillales and Alteromonadales
•Suggests the identities of bacterial groups affected under the ocean trend of pollution, deoxygenation and acidification
Anthropogenic nutrient enrichment results in hypoxia, ocean acidification and elevated nutrients (HOAN) in coastal environments throughout the world. Here, we examined the composition of biofilm bacterial communities from a nutrient-excessive fish farm with low dissolved oxygen (DO) and pH levels using 16S rRNA gene sequencing. HOAN was accompanied by higher bacterial diversity and richness, and resulted in an altered community composition than the control site. HOAN resulted in more Flavobacteriales, Rhizobiales, Epsilonproteobacteria and Vibrionales, but less Oceanospirillales and Alteromonadales. Photobacterium sp. and Vibrio sp. were mostly found to be exclusive to HOAN conditions, suggesting that HOAN could possibly proliferate the presence of these potential pathogens. Our study suggests the complexity of bacterial communities to hypoxia and acidification in response to increased nutrient loads, along with identities of nutrient, oxygen and pH-susceptible bacterial groups that are most likely affected under this ocean trend.
•Low pH, low DO and high temperature showed drastic effects on digestive enzyme activities.
•Low pH, low DO and high temperature synergistically reduced digestive enzyme activities.
•Lysozyme showed increased and then decreased activities with time.
•Combinations of low pH, low DO and high temperature showed more severe effects on digestive enzymes than single factors.
•Hypoxia and high temperature showed similar effects on digestive enzyme activities.
Global change and anthropogenic activities have driven marine environment changes dramatically during the past century, and hypoxia, acidification and warming have received much attention recently. Yet, the interactive effects among these stressors on marine organisms are extremely complex and not accurately clarified. Here, we evaluated the combined effects of low dissolved oxygen (DO), low pH and warming on the digestive enzyme activities of the mussel Mytilus coruscus. In this experiment, mussels were exposed to eight treatments, including two degrees of pH (8.1, 7.7), DO (6, 2 mg/l) and temperature (30 °C and 20 °C) for 30 days. Amylase (AMS), lipase (LPS), trypsin (TRY), trehalase (TREH) and lysozyme (LZM) activities were measured in the digestive glands of mussels. All the tested stress conditions showed significant effects on the enzymatic activities. AMS, LPS, TRY, TREH showed throughout decreased trend in their activities due to low pH, low DO, increased temperature and different combinations of these three stressors with time but LZM showed increased and then decreased trend in their activities. Hypoxia and warming showed almost similar effects on the enzymatic activities. PCA showed a positive correlation among all measured biochemical parameters. Therefore, the fitness of mussel is likely impaired by such marine environmental changes and their population may be affected under the global change scenarios.
Climate change can have a pronounced impact on the physiology and behaviour of fishes. Notably, many climate change stressors, such as global warming, hypoxia and ocean acidification (OA), have been shown to alter the kinematics of predator–prey interactions in fishes, with potential effects at ecological levels. Here, we review the main effects of each of these stressors on fish escape responses using an integrative approach that encompasses behavioural and kinematic variables. Elevated temperature was shown to affect many components of the escape response, including escape latencies, kinematics and maximum swimming performance, while the main effect of hypoxia was on escape responsiveness and directionality. OA had a negative effect on the escape response of juvenile fish by decreasing their directionality, responsiveness and locomotor performance, although some studies show no effect of acidification. The few studies that have explored the effects of multiple stressors show that temperature tends to have a stronger effect on escape performance than OA. Overall, the effects of climate change on escape responses may occur through decreased muscle performance and/or an interference with brain and sensory functions. In all of these cases, since the escape response is a behaviour directly related to survival, these effects are likely to be fundamental drivers of changes in marine communities. The overall future impact of these stressors is discussed by including their potential effects on predator attack behaviour, thereby allowing the development of potential future scenarios for predator–prey interactions.
• Gill metabolism of king scallops is affected by singly and combined climate drivers
• Scallops were most tolerant to warming plus hypercapnia and were most susceptible to oxygen reduction
• Metabolic analysis revealed alterations in mitochondrial energy metabolism most pronounced in scallops exposed to high temperatures and Deadly trio (Warming + hypercapnia + hypoxia)
• Imbalances in energy metabolism decrease the upper thermal tolerance of P. maximus
In the ocean the main climate drivers affecting marine organisms are warming, hypercapnia, and hypoxia. We investigated the acute effects of warming (W), warming plus hypercapnia (WHc, ~1800 μatm CO2), warming plus hypoxia (WHo, ~12.1 kPa O2), and a combined exposure of all three drivers (Deadly Trio, DT) on king scallops (Pecten maximus). All exposures started at 14 °C and temperature was increased by 2 °C once every 48 h until the lethal temperature was reached (28 °C). Gill samples were taken at 14 °C, 18 °C, 22 °C, and 26 °C and analyzed for their metabolic response by 1H-nuclear magnetic resonance (NMR) spectroscopy. Scallops were most tolerant to WHc and most susceptible to oxygen reduction (WHo and DT). In particular under DT, scallops’ mitochondrial energy metabolism was affected. Changes became apparent at 22 °C and 26 °C involving significant accumulation of glycogenic amino acids (e.g. glycine and valine) and anaerobic end-products (e.g. acetic acid and succinate). In line with these observations the LT50 was lower under the exposure to DT (22.5 °C) than to W alone (~ 25 °C) indicating a narrowing of the thermal niche due to an imbalance between oxygen demand and supply.
Species interactions are crucial for the persistence of ecosystems. Within vegetated habitats, early life stages of plants and algae must survive factors such as grazing to recover from disturbances. However, grazing impacts on early stages, especially under the context of a rapidly changing climate, are largely unknown. Here we examine interaction strengths between juvenile giant kelp (Macrocystis pyrifera) and four common grazers under hypoxia and ocean acidification using short-term laboratory experiments and field data of grazer abundances to estimate population-level grazing impacts. We found that grazing is a significant source of mortality for juvenile kelp and, using field abundances, estimate grazers can remove on average 15.4% and a maximum of 73.9% of juveniles per m2 per day. Short-term exposure to low oxygen, not acidification, weakened interaction strengths across the four species and decreased estimated population-level impacts of grazing threefold, from 15.4% to 4.0% of juvenile kelp removed, on average, per m2 per day. This study highlights potentially high juvenile kelp mortality from grazing. We also show that the effects of hypoxia are stronger than the effects of acidification in weakening these grazing interactions over short timescales, with possible future consequences for the persistence of giant kelp and energy flow through these highly productive food webs.
• The combined effects of acidification and hypoxia on physiological performance of mussels were investigated.
• Diel fluctuating hypoxia and acidification had less impact on the internal environment of mussels compared with constant exposure.
• Mussels had higher growth performance under diel cycling acidification and hypoxia compared with constant exposure.
• Mussels showed stronger resistance to diel cycling seawater acidification and hypoxia than constant exposure.
Ocean acidification and hypoxia are concurrent in some coastal waters due to anthropogenic activities in the past decades. In the natural environment, pH and dissolved oxygen (DO) may fluctuate and follow diel-cycling patterns, but such effects on marine animals have not been comprehensively studied compared to their constant effects. In order to study the effects of diel-cycling seawater acidification and hypoxia on the fitness of marine bivalves, the thick shell mussels Mytilus coruscus were exposed to two constant levels of dissolved oxygen (2 mg/L, 8 mg/L) under two pH treatments (7.3, 8.1), as well as single diel fluctuating pH or DO, and the combined diel fluctuating of pH and DO for three weeks. The experimental results showed that constant acidification and hypoxia significantly reduced the extracellular pH (pHe) and condition index (CI) of mussels, and significantly increased HCO3−, pCO2 and standard metabolic rate (SMR). Diel fluctuating hypoxia and acidification also significantly reduced the pHe and CI, and significantly increased pCO2 and SMR, but had no significant effects on HCO3−. However, the diel-cycling acidification and hypoxia resulted in a higher CI compared to continuous exposure. In general, continuous and intermittent stress negatively impact the hemolymph and growth performance of mussels. However, mussels possess a little stronger resistance to diel-cycling seawater acidification and hypoxia than sustained stress.