Ocean acidification boosts reproduction in fish via indirect effects

Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO₂ are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO₂ vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO₂ on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO₂ vents, which may further boost reproductive success. These positive indirect effects of elevated CO₂ were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean.

Ocean acidification affects species populations and diversity through direct negative effects on physiology and behavior, but the indirect effects are less clear. Using volcanic carbon dioxide vents as natural analogues of future ocean acidification, this study shows that elevated CO2 can stimulate fish reproduction in the wild through increased food abundance, leading to increased energy budgets at no cost to physiological homeostasis.     

Natural acidification changes the timing and rate of succession,alters community structure,and increases homogeneity in marine biofouling communities

Ocean acidification may have far‐reaching consequences for marine community and ecosystem dynamics, but its full impacts remain poorly understood due to the difficulty of manipulating pCO₂ at the ecosystem level to mimic realistic fluctuations that occur on a number of different timescales. It is especially unclear how quickly communities at various stages of development respond to intermediate‐scale pCO₂ change and, if high pCO₂ is relieved mid‐succession, whether past acidification effects persist, are reversed by alleviation of pCO₂ stress, or are worsened by departures from prior high pCO₂ conditions to which organisms had acclimatized. Here, we used reciprocal transplant experiments along a shallow water volcanic pCO₂ gradient to assess the importance of the timing and duration of high pCO₂ exposure (i.e., discrete events at different stages of successional development vs. continuous exposure) on patterns of colonization and succession in a benthic fouling community. We show that succession at the acidified site was initially delayed (less community change by 8 weeks) but then caught up over the next 4 weeks. These changes in succession led to homogenization of communities maintained in or transplanted to acidified conditions, and altered community structure in ways that reflected both short‐ and longer‐term acidification history. These community shifts are likely a result of interspecific variability in response to increased pCO₂ and changes in species interactions. High pCO₂ altered biofilm development, allowing serpulids to do best at the acidified site by the end of the experiment, although early (pretransplant) negative effects of pCO₂ on recruitment of these worms were still detectable. The ascidians Diplosoma sp. and Botryllus sp. settled later and were more tolerant to acidification. Overall, transient and persistent acidification‐driven changes in the biofouling community, via both past and more recent exposure, could have important implications for ecosystem function and food web dynamics.     

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

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

Regulation of gene expression is associated with tolerance of the Arctic copepod Calanus glacialis to CO2‐acidified sea water

Ocean acidification is the increase in seawater pCO₂ due to the uptake of atmospheric anthropogenic CO₂, with the largest changes predicted to occur in the Arctic seas. For some marine organisms, this change in pCO₂, and associated decrease in pH, represents a climate change‐related stressor. In this study, we investigated the gene expression patterns of nauplii of the Arctic copepod Calanus glacialis cultured at low pH levels. We have previously shown that organismal‐level performance (development, growth, respiration) of C. glacialis nauplii is unaffected by low pH. Here, we investigated the molecular‐level response to lowered pH in order to elucidate the physiological processes involved in this tolerance. Nauplii from wild‐caught C. glacialis were cultured at four pH levels (8.05, 7.9, 7.7, 7.5). At stage N6, mRNA was extracted and sequenced using RNA‐seq. The physiological functionality of the proteins identified was categorized using Gene Ontology and KEGG pathways. We found that the expression of 151 contigs varied significantly with pH on a continuous scale (93% downregulated with decreasing pH). Gene set enrichment analysis revealed that, of the processes downregulated, many were components of the universal cellular stress response, including DNA repair, redox regulation, protein folding, and proteolysis. Sodium:proton antiporters were among the processes significantly upregulated, indicating that these ion pumps were involved in maintaining cellular pH homeostasis. C. glacialis significantly alters its gene expression at low pH, although they maintain normal larval development. Understanding what confers tolerance to some species will support our ability to predict the effects of future ocean acidification on marine organisms.     

EVOLUTIONARY RESPONSES OF A COCCOLITHOPHORID GEPHYROCAPSA OCEANICA TO OCEAN ACIDIFICATION

The ongoing ocean acidification associated with a changing carbonate system may impose profound effects on marine planktonic calcifiers. Here, we show that a coccolithophore, Gephyrocapsa oceanica, evolved in response to an elevated CO₂ concentration of 1000 μatm (pH reduced to 7.8) in a long‐term (～670 generations) selection experiment. The high CO₂‐selected cells showed increases in photosynthetic carbon fixation, growth rate, cellular particulate organic carbon (POC) or nitrogen (PON) production, and a decrease in C:N elemental ratio, indicating a greater upregulation of PON than of POC production under the ocean acidification condition. Cells from the low CO₂ selection process shifted to high CO₂ exposure showed an enhanced cellular POC and PON production rates. Our data suggest that the coccolithophorid could adapt to ocean acidification with enhanced assimilations of carbon and nitrogen but decreased C:N ratios.     

Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and pCO2

Increased atmospheric pCO₂ is expected to render future oceans warmer and more acidic than they are at present. Calcifying organisms such as coccolithophores that fix and export carbon into the deep sea provide feedbacks to increasing atmospheric pCO₂. Acclimation experiments suggest negative effects of warming and acidification on coccolithophore calcification, but the ability of these organisms to adapt to future environmental conditions is not well understood. Here, we tested the combined effect of pCO₂ and temperature on the coccolithophore Emiliania huxleyi over more than 700 generations. Cells increased inorganic carbon content and calcification rate under warm and acidified conditions compared with ambient conditions, whereas organic carbon content and primary production did not show any change. In contrast to findings from short-term experiments, our results suggest that long-term acclimation or adaptation could change, or even reverse, negative calcification responses in E. huxleyi and its feedback to the global carbon cycle. Genome-wide profiles of gene expression using RNA-seq revealed that genes thought to be essential for calcification are not those that are most strongly differentially expressed under long-term exposure to future ocean conditions. Rather, differentially expressed genes observed here represent new targets to study responses to ocean acidification and warming.     

Echinometra sea urchins acclimatized to elevated pCO2 at volcanic vents outperform those under present‐day pCO2 conditions

Rising atmospheric CO₂ concentrations will significantly reduce ocean pH during the 21st century (ocean acidification, OA). This may hamper calcification in marine organisms such as corals and echinoderms, as shown in many laboratory‐based experiments. Sea urchins are considered highly vulnerable to OA. We studied an Echinometra species on natural volcanic CO₂ vents in Papua New Guinea, where they are CO₂‐acclimatized and also subjected to secondary ecological changes from elevated CO₂. Near the vent site, the urchins experienced large daily variations in pH (>1 unit) and pCO₂ (>2000 ppm) and average pH values (pH_T 7.73) much below those expected under the most pessimistic future emission scenarios. Growth was measured over a 17‐month period using tetracycline tagging of the calcareous feeding lanterns. Average‐sized urchins grew more than twice as fast at the vent compared with those at an adjacent control site and assumed larger sizes at the vent compared to the control site and two other sites at another reef near‐by. A small reduction in gonad weight was detected at the vents, but no differences in mortality, respiration, or degree of test calcification were detected between urchins from vent and control populations. Thus, urchins did not only persist but actually ‘thrived’ under extreme CO₂ conditions. We suggest an ecological basis for this response: Increased algal productivity under increased pCO₂ provided more food at the vent, resulting in higher growth rates. The wider implication of our observation is that laboratory studies on non‐acclimatized specimens, which typically do not consider ecological changes, can lead to erroneous conclusions on responses to global change.     

The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance

Predictions concerning the consequences of the oceanic uptake of increasing atmospheric carbon dioxide (CO₂) have been primarily occupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks direct and indirect effects of CO₂ on non-calcareous taxa that play critical roles in ecosystem shifts (e.g. competitors). We present the model that future atmospheric [CO₂] may act as a resource for mat-forming algae, a diverse and widespread group known to reduce the resilience of kelp forests and coral reefs. We test this hypothesis by combining laboratory and field CO₂ experiments and data from ‘natural’ volcanic CO₂ vents. We show that mats have enhanced productivity in experiments and more expansive covers in situ under projected near-future CO₂ conditions both in temperate and tropical conditions. The benefits of CO₂ are likely to vary among species of producers, potentially leading to shifts in species dominance in a high CO₂ world. We explore how ocean acidification combines with other environmental changes across a number of scales, and raise awareness of CO₂ as a resource whose change in availability could have wide-ranging community consequences beyond its direct effects.     

Temperate and tropical brown macroalgae thrive,despite decalcification,along natural CO2 gradients

Predicting the impacts of ocean acidification on coastal ecosystems requires an understanding of the effects on macroalgae and their grazers, as these underpin the ecology of rocky shores. Whilst calcified coralline algae (Rhodophyta) appear to be especially vulnerable to ocean acidification, there is a lack of information concerning calcified brown algae (Phaeophyta), which are not obligate calcifiers but are still important producers of calcium carbonate and organic matter in shallow coastal waters. Here, we compare ecological shifts in subtidal rocky shore systems along CO₂ gradients created by volcanic seeps in the Mediterranean and Papua New Guinea, focussing on abundant macroalgae and grazing sea urchins. In both the temperate and tropical systems the abundances of grazing sea urchins declined dramatically along CO₂ gradients. Temperate and tropical species of the calcifying macroalgal genus Padina (Dictyoaceae, Phaeophyta) showed reductions in CaCO₃ content with CO₂ enrichment. In contrast to other studies of calcified macroalgae, however, we observed an increase in the abundance of Padina spp. in acidified conditions. Reduced sea urchin grazing pressure and significant increases in photosynthetic rates may explain the unexpected success of decalcified Padina spp. at elevated levels of CO₂. This is the first study to provide a comparison of ecological changes along CO₂ gradients between temperate and tropical rocky shores. The similarities we found in the responses of Padina spp. and sea urchin abundance at several vent systems increases confidence in predictions of the ecological impacts of ocean acidification over a large geographical range .     

Responses of the Emiliania huxleyi Proteome to Ocean Acidification

Ocean acidification due to rising atmospheric CO₂ is expected to affect the physiology of important calcifying marine organisms, but the nature and magnitude of change is yet to be established. In coccolithophores, different species and strains display varying calcification responses to ocean acidification, but the underlying biochemical properties remain unknown. We employed an approach combining tandem mass-spectrometry with isobaric tagging (iTRAQ) and multiple database searching to identify proteins that were differentially expressed in cells of the marine coccolithophore species Emiliania huxleyi (strain NZEH) between two CO₂ conditions: 395 (∼current day) and ∼1340 p.p.m.v. CO₂. Cells exposed to the higher CO₂ condition contained more cellular particulate inorganic carbon (CaCO₃) and particulate organic nitrogen and carbon than those maintained in present-day conditions. These results are linked with the observation that cells grew slower under elevated CO₂, indicating cell cycle disruption. Under high CO₂ conditions, coccospheres were larger and cells possessed bigger coccoliths that did not show any signs of malformation compared to those from cells grown under present-day CO₂ levels. No differences in calcification rate, particulate organic carbon production or cellular organic carbon: nitrogen ratios were observed. Results were not related to nutrient limitation or acclimation status of cells. At least 46 homologous protein groups from a variety of functional processes were quantified in these experiments, of which four (histones H2A, H3, H4 and a chloroplastic 30S ribosomal protein S7) showed down-regulation in all replicates exposed to high CO₂, perhaps reflecting the decrease in growth rate. We present evidence of cellular stress responses but proteins associated with many key metabolic processes remained unaltered. Our results therefore suggest that this E. huxleyi strain possesses some acclimation mechanisms to tolerate future CO₂ scenarios, although the observed decline in growth rate may be an overriding factor affecting the success of this ecotype in future oceans.     

The physiological response of marine diatoms to ocean acidification: differential roles of seawater pCO2 and pH

Although increasing the pCO₂ for diatoms will presumably down‐regulate the CO₂‐concentrating mechanism (CCM) to save energy for growth, different species have been reported to respond differently to ocean acidification (OA). To better understand their growth responses to OA, we acclimated the diatoms Thalassiosira pseudonana, Phaeodactylum tricornutum, and Chaetoceros muelleri to ambient (pCO₂ 400 μatm, pH 8.1), carbonated (pCO₂ 800 μatm, pH 8.1), acidified (pCO₂ 400 μatm, pH 7.8), and OA (pCO₂ 800 μatm, pH 7.8) conditions and investigated how seawater pCO₂ and pH affect their CCMs, photosynthesis, and respiration both individually and jointly. In all three diatoms, carbonation down‐regulated the CCMs, while acidification increased both the photosynthetic carbon fixation rate and the fraction of CO₂ as the inorganic carbon source. The positive OA effect on photosynthetic carbon fixation was more pronounced in C. muelleri, which had a relatively lower photosynthetic affinity for CO₂, than in either T. pseudonana or P. tricornutum. In response to OA, T. pseudonana increased respiration for active disposal of H⁺ to maintain its intracellular pH, whereas P. tricornutum and C. muelleri retained their respiration rate but lowered the intracellular pH to maintain the cross‐membrane electrochemical gradient for H⁺ efflux. As the net result of changes in photosynthesis and respiration, growth enhancement to OA of the three diatoms followed the order of C. muelleri > P. tricornutum > T. pseudonana. This study demonstrates that elucidating the separate and joint impacts of increased pCO₂ and decreased pH aids the mechanistic understanding of OA effects on diatoms in the future, acidified oceans.     

Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification

Coccolithophores are unicellular marine algae that produce biogenic calcite scales and substantially contribute to marine primary production and carbon export to the deep ocean. Ongoing ocean acidification particularly impairs calcifying organisms, mostly resulting in decreased growth and calcification. Recent studies revealed that the immediate physiological response in the coccolithophore Emiliania huxleyi to ocean acidification may be partially compensated by evolutionary adaptation, yet the underlying molecular mechanisms are currently unknown. Here, we report on the expression levels of 10 candidate genes putatively relevant to pH regulation, carbon transport, calcification and photosynthesis in E. huxleyi populations short-term exposed to ocean acidification conditions after acclimation (physiological response) and after 500 generations of high CO₂ adaptation (adaptive response). The physiological response revealed downregulation of candidate genes, well reflecting the concomitant decrease of growth and calcification. In the adaptive response, putative pH regulation and carbon transport genes were up-regulated, matching partial restoration of growth and calcification in high CO₂-adapted populations. Adaptation to ocean acidification in E. huxleyi likely involved improved cellular pH regulation, presumably indirectly affecting calcification. Adaptive evolution may thus have the potential to partially restore cellular pH regulatory capacity and thereby mitigate adverse effects of ocean acidification.     

Vacuolar acidification in Saccharomyces cerevisiae induced by elevated hydrostatic pressure is transient and is mediated by vacuolar H+-ATPase

We analyzed the vacuolar acidification in response to elevated hydrostatic pressure in Saccharomyces cerevisiae. The vacuolar pH, defined using 6-carboxyfluorescein, was directly measured in a hyperbaric chamber with a transparent window under high hydrostatic pressure. The vacuole of strain X2180 became acidified at the onset of pressurization to an extent dependent on the magnitude of pressure applied. A pressure of 40–60 MPa transiently reduced the vacuolar pH by about 0.33 within 4 min. The transient acidification was observed in the presence of D-glucose, D-fructose, or D-mannose as a carbon source, but not 3-o-methyl-D-glucose, ethanol, or glycerol, suggesting that the generation of CO₂ was involved in the process. A vma3 mutant defective in vacuolar acidification showed no reduction of vacuolar pH when hydrostatic pressure was applied. This result indicates that the transient vacuolar acidification induced by elevated hydrostatic pressure is mediated through the function of the vacuolar H+-ATPase. Received: August 21, 1996 / Accepted: November 11, 1996     

Combined effects of ocean acidification and solar UV radiation on photosynthesis,growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta)

Previous studies have shown that increasing atmospheric CO₂ concentrations affect calcification in some planktonic and macroalgal calcifiers due to the changed carbonate chemistry of seawater. However, little is known regarding how calcifying algae respond to solar UV radiation (UVR, UVA+UVB, 280–400 nm). UVR may act synergistically, antagonistically or independently with ocean acidification (high CO₂/low pH of seawater) to affect their calcification processes. We cultured the articulated coralline alga Corallina sessilis Yendo at 380 ppmv (low) and 1000 ppmv (high) CO₂ levels while exposing the alga to solar radiation treatments with or without UVR. The presence of UVR inhibited the growth, photosynthetic O₂ evolution and calcification rates by13%, 6% and 3% in the low and by 47%, 20% and 8% in the high CO₂ concentrations, respectively, reflecting a synergistic effect of CO₂ enrichment with UVR. UVR induced significant decline of pH in the CO₂‐enriched cultures. The contents of key photosynthetic pigments, chlorophyll a and phycobiliproteins decreased, while UV‐absorptivity increased under the high pCO₂/low pH condition. Nevertheless, UV‐induced inhibition of photosynthesis increased when the ratio of particulate inorganic carbon/particulate organic carbon decreased under the influence of CO₂‐acidified seawater, suggesting that the calcified layer played a UV‐protective role. Both UVA and UVB negatively impacted photosynthesis and calcification, but the inhibition caused by UVB was about 2.5–2.6 times that caused by UVA. The results imply that coralline algae suffer from more damage caused by UVB as they calcify less and less with progressing ocean acidification.     

Alterations of Intracellular pH in Response to Low Temperature Stresses

+ -ATPase is one of the primary cellular events directly resulting from cold exposure. We demonstrate here that cold-induced inactivation of the proton translocating enzyme is closely linked to the rapid acidification of the cytoplasm and the concomitant alkalization of the vacuoles, suggesting an important role of the enzyme in maintaining homeostasis of the cellular pH in a cold environment. The stability of the vacuolar H⁺-ATPase to cold both in vivo and in vitro is distinctly different between species sensitive and insensitive to cold. These findings provide further insight into the way in which the vacuolar H⁺-ATPase is involved in cold adaptation of plants. In addition, the temperature reduction and the concentration of the cytoplasm as a consequence of freeze-induced dehydration may also result in changes in the cellular pH. In fact, we demonstrate here that the cytoplasm is markedly acidified upon freezing; in particular, in cells of less hardy plants. Freeze-induced acidification is presumably due to changes in the physico-chemical properties of the cytoplasm and the changes in the permeability of the vacuolar membrane both of which result from severe dehydration. The physiological significance of freeze-induced acidification of the cytoplasm is discussed. Received 26 March 1999/ Accepted in revised form 30 March 1999