Multilayer biological networks to upscale marine research to global change-smart management and sustainable resource use.

Human activities are having a massive negative impact on biodiversity and ecological processes worldwide. The rate and magnitude of ecological transformations induced by climate change, habitat destruction, overexploitation and pollution are now so substantial that a sixth mass extinction event is currently underway. The biodiversity crisis of the Anthropocene urges scientists to put forward a transformative vision to promote the conservation of biodiversity, and thus indirectly the preservation of ecosystem functions. Here, we identify pressing issues in global change biology research and propose an integrative framework based on multilayer biological networks as a tool to support conservation actions and marine risk assessments in multi-stressor scenarios. Multilayer networks can integrate different levels of environmental and biotic complexity, enabling us to combine information on molecular, physiological and behaviour responses, species interactions and biotic communities. The ultimate aim of this framework is to link human-induced environmental changes to species physiology, fitness, biogeography and ecosystem impacts across vast seascapes and time frames, to help guide solutions to address biodiversity loss and ecological tipping points. Further, we also define our current ability to adopt a widespread use of multilayer networks within ecology, evolution and conservation by providing examples of case-studies. We also assess which approaches are ready to be transferred and which ones require further development before use. We conclude that multilayer biological networks will be crucial to inform (using reliable multi-levels integrative indicators) stakeholders and support their decision-making concerning the sustainable use of resources and marine conservation.

Ocean acidification and hypoxia alter organic carbon fluxes in marine soft sediments.

Anthropogenic stressors can alter the structure and functioning of infaunal communities, which are key drivers of the carbon cycle in marine soft sediments. Nonetheless, the compounded effects of anthropogenic stressors on carbon fluxes in soft benthic systems remain largely unknown. Here, we investigated the cumulative effects of ocean acidification (OA) and hypoxia on the organic carbon fate in marine sediments, through a mesocosm experiment. Isotopically labelled macroalgal detritus (13 C) was used as a tracer to assess carbon incorporation in faunal tissue and in sediments under different experimental conditions. In addition, labelled macroalgae (13 C), previously exposed to elevated CO2 , were also used to assess the organic carbon uptake by fauna and sediments, when both sources and consumers were exposed to elevated CO2 . At elevated CO2 , infauna increased the uptake of carbon, likely as compensatory response to the higher energetic costs faced under adverse environmental conditions. By contrast, there was no increase in carbon uptake by fauna exposed to both stressors in combination, indicating that even a short-term hypoxic event may weaken the ability of marine invertebrates to withstand elevated CO2 conditions. In addition, both hypoxia and elevated CO2 increased organic carbon burial in the sediment, potentially affecting sediment biogeochemical processes. Since hypoxia and OA are predicted to increase in the face of climate change, our results suggest that local reduction of hypoxic events may mitigate the impacts of global climate change on marine soft-sediment systems.

Acid-base physiology over tidal periods in the mussel Mytilus edulis: size and temperature are more influential than seawater pH.

Ocean acidification (OA) studies to date have typically used stable open-ocean pH and CO2 values to predict the physiological responses of intertidal species to future climate scenarios, with few studies accounting for natural fluctuations of abiotic conditions or the alternating periods of emersion and immersion routinely experienced during tidal cycles. Here, we determine seawater carbonate chemistry and the corresponding in situ haemolymph acid-base responses over real time for two populations of mussel ( Mytilus edulis) during tidal cycles, demonstrating that intertidal mussels experience daily acidosis during emersion. Using these field data to parameterize experimental work we demonstrate that air temperature and mussel size strongly influence this acidosis, with larger mussels at higher temperatures experiencing greater acidosis. There was a small interactive effect of prior immersion in OA conditions (pHNBS 7.7/pCO2 930 µatm) such that the haemolymph pH measured at the start of emersion was lower in large mussels exposed to OA. Critically, the acidosis induced in mussels during emersion in situ was greater (ΔpH approximately 0.8 units) than that induced by experimental OA (ΔpH approximately 0.1 units). Understanding how environmental fluctuations influence physiology under current scenarios is critical to our ability to predict the responses of key marine biota to future environmental changes.

Assessing the living and dead proportions of cold-water coral colonies: implications for deep-water Marine Protected Area monitoring in a changing ocean.

Coral growth patterns result from an interplay of coral biology and environmental conditions. In this study colony size and proportion of live and dead skeletons in the cold-water coral (CWC) Lophelia pertusa (Linnaeus, 1758) were measured using video footage from Remotely Operated Vehicle (ROV) transects conducted at the inshore Mingulay Reef Complex (MRC) and at the offshore PISCES site (Rockall Bank) in the NE Atlantic. The main goal of this paper was to explore the development of a simple method to quantify coral growth and its potential application as an assessment tool of the health of these remote habitats. Eighteen colonies were selected and whole colony and dead/living layer size were measured. Live to dead layer ratios for each colony were then determined and analysed. The age of each colony was estimated using previously published data. Our paper shows that: (1) two distinct morphotypes can be described: at the MRC, colonies displayed a 'cauliflower-shaped' morphotype whereas at the PISCES site, colonies presented a more flattened 'bush-shaped' morphotype; (2) living layer size was positively correlated with whole colony size; (3) live to dead layer ratio was negatively correlated to whole colony size; (4) live to dead layer ratio never exceeded 0.27. These results suggest that as a colony develops and its growth rate slows down, the proportion of living polyps in the colony decreases. Furthermore, at least 73% of L. pertusa colonies are composed of exposed dead coral skeleton, vulnerable to ocean acidification and the associated shallowing of the aragonite saturation horizon, with significant implications for future deep-sea reef framework integrity. The clear visual contrast between white/pale living and grey/dark dead portions of the colonies also gives a new way by which they can be visually monitored over time. The increased use of marine autonomous survey vehicles offers an important new platform from which such a surveying technique could be applied to monitor deep-water marine protected areas in the future.

Fluctuating seawater pH/pCO2 regimes are more energetically expensive than static pH/pCO2 levels in the mussel Mytilus edulis.

Ocean acidification (OA) studies typically use stable open-ocean pH or CO2 values. However, species living within dynamic coastal environments can naturally experience wide fluctuations in abiotic factors, suggesting their responses to stable pH conditions may not be reflective of either present or near-future conditions. Here we investigate the physiological responses of the mussel Mytilus edulis to variable seawater pH conditions over short- (6 h) and medium-term (2 weeks) exposures under both current and near-future OA scenarios. Mussel haemolymph pH closely mirrored that of seawater pH over short-term changes of 1 pH unit with acidosis or recovery accordingly, highlighting a limited capacity for acid-base regulation. After 2 weeks, mussels under variable pH conditions had significantly higher metabolic rates, antioxidant enzyme activities and lipid peroxidation than those exposed to static pH under both current and near-future OA scenarios. Static near-future pH conditions induced significant acid-base disturbances and lipid peroxidation compared with the static present-day conditions but did not affect the metabolic rate. These results clearly demonstrate that living in naturally variable environments is energetically more expensive than living in static seawater conditions, which has consequences for how we extrapolate future OA responses in coastal species.

Effects of elevated CO2 on phytoplankton community biomass and species composition during a spring Phaeocystis spp. bloom in the western English Channel.

A 21-year time series of phytoplankton community structure was analysed in relation to Phaeocystis spp. to elucidate its contribution to the annual carbon budget at station L4 in the western English Channel (WEC). Between 1993-2014 Phaeocystis spp. contributed ∼4.6% of the annual phytoplankton carbon and during the March - May spring bloom, the mean Phaeocystis spp. biomass constituted 17% with a maximal contribution of 47% in 2001. Upper maximal weekly values above the time series mean ranged from 63 to 82% of the total phytoplankton carbon (∼42-137mg carbon (C)m-3) with significant inter-annual variability in Phaeocystis spp. Maximal biomass usually occurred by the end of April, although in some cases as early as mid-April (2007) and as late as late May (2013). The effects of elevated pCO2 on the Phaeocystis spp. spring bloom were investigated during a fifteen-day semi-continuous microcosm experiment. The phytoplankton community biomass was estimated at ∼160mgCm-3 and was dominated by nanophytoplankton (40%, excluding Phaeocystis spp.), Phaeocystis spp. (30%) and cryptophytes (12%). The smaller fraction of the community biomass comprised picophytoplankton (9%), coccolithophores (3%), Synechococcus (3%), dinoflagellates (1.5%), ciliates (1%) and diatoms (0.5%). Over the experimental period, total biomass increased significantly by 90% to ∼305mgCm-3 in the high CO2 treatment while the ambient pCO2 control showed no net gains. Phaeocystis spp. exhibited the greatest response to the high CO2 treatment, increasing by 330%, from ∼50mgCm-3 to over 200mgCm-3 and contributing ∼70% of the total biomass. Taken together, the results of our microcosm experiment and analysis of the time series suggest that a future high CO2 scenario may favour dominance of Phaeocystis spp. during the spring bloom. This has significant implications for the formation of hypoxic zones and the alteration of food web structure including inhibitory feeding effects and lowered fecundity in many copepod species.

Elevated CO2 induces a bloom of microphytobenthos within a shell gravel mesocosm.

The geological storage of carbon dioxide (CO2) is expected to be an important component of future global carbon emission mitigation, but there is a need to understand the impacts of a CO2 leak on the marine environment and to develop monitoring protocols for leakage detection. In the present study, sediment cores were exposed to CO2-acidified seawater at one of five pH levels (8.0, 7.5, 7.0, 6.5 and 6.0) for 10 weeks. A bloom of Spirulina sp. and diatoms appeared on sediment surface exposed to pH 7.0 and 7.5 seawater. Quantitative PCR measurements of the abundance of 16S rRNA also indicated an increase within the pH 7.0 and 7.5 treatments after 10 weeks incubation. More detailed analysis of the microbial communities from the pH 7.0, 7.5 and 8.0 treatments confirmed an increase in the relative abundance of Spirulina sp. and Navicula sp. sequences, with changes in the relative abundance of major archaeal and bacterial groups also detected within the pH 7.0 treatment. A decreased flux of silicate from the sediment at this pH was also detected. Monitoring blooms of microphytobenthos may prove useful as an indicator of CO2 leakage within coastal areas.

Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem.

Understanding long-term, ecosystem-level impacts of climate change is challenging because experimental research frequently focuses on short-term, individual-level impacts in isolation. We address this shortcoming first through an interdisciplinary ensemble of novel experimental techniques to investigate the impacts of 14-month exposure to ocean acidification and warming (OAW) on the physiology, activity, predatory behaviour and susceptibility to predation of an important marine gastropod (Nucella lapillus). We simultaneously estimated the potential impacts of these global drivers on N. lapillus population dynamics and dispersal parameters. We then used these data to parameterize a dynamic bioclimatic envelope model, to investigate the consequences of OAW on the distribution of the species in the wider NE Atlantic region by 2100. The model accounts also for changes in the distribution of resources, suitable habitat and environment simulated by finely resolved biogeochemical models, under three IPCC global emissions scenarios. The experiments showed that temperature had the greatest impact on individual-level responses, while acidification had a similarly important role in the mediation of predatory behaviour and susceptibility to predators. Changes in Nucella predatory behaviour appeared to serve as a strategy to mitigate individual-level impacts of acidification, but the development of this response may be limited in the presence of predators. The model projected significant large-scale changes in the distribution of Nucella by the year 2100 that were exacerbated by rising greenhouse gas emissions. These changes were spatially heterogeneous, as the degree of impact of OAW on the combination of responses considered by the model varied depending on local-environmental conditions and resource availability. Such changes in macro-scale distributions cannot be predicted by investigating individual-level impacts in isolation, or by considering climate stressors separately. Scaling up the results of experimental climate change research requires approaches that account for long-term, multiscale responses to multiple stressors, in an ecosystem context.

Late winter under ice pelagic microbial communities in the high Arctic Ocean and the impact of short-term exposure to elevated CO2 levels.

Polar Oceans are natural CO2 sinks because of the enhanced solubility of CO2 in cold water. The Arctic Ocean is at additional risk of accelerated ocean acidification (OA) because of freshwater inputs from sea ice and rivers, which influence the carbonate system. Winter conditions in the Arctic are of interest because of both cold temperatures and limited CO2 venting to the atmosphere when sea ice is present. Earlier OA experiments on Arctic microbial communities conducted in the absence of ice cover, hinted at shifts in taxa dominance and diversity under lowered pH. The Catlin Arctic Survey provided an opportunity to conduct in situ, under-ice, OA experiments during late Arctic winter. Seawater was collected from under the sea ice off Ellef Ringnes Island, and communities were exposed to three CO2 levels for 6 days. Phylogenetic diversity was greater in the attached fraction compared to the free-living fraction in situ, in the controls and in the treatments. The dominant taxa in all cases were Gammaproteobacteria but acidification had little effect compared to the effects of containment. Phylogenetic net relatedness indices suggested that acidification may have decreased the diversity within some bacterial orders, but overall there was no clear trend. Within the experimental communities, alkalinity best explained the variance among samples and replicates, suggesting subtle changes in the carbonate system need to be considered in such experiments. We conclude that under ice communities have the capacity to respond either by selection or phenotypic plasticity to heightened CO2 levels over the short term.

Environmental variability and biodiversity of megabenthos on the Hebrides Terrace Seamount (Northeast Atlantic).

We present the first remotely operated vehicle investigation of megabenthic communities (1004-1695 m water depth) on the Hebrides Terrace Seamount (Northeast Atlantic). Conductivity-temperature-depth casts showed rapid light attenuation below the summit and an oceanographic regime on the flanks consistent with an internal tide, and high short-term variability in water temperature, salinity, light attenuation, aragonite and oxygen down to 1500 m deep. Minor changes in species composition (3-14%) were explained by changes in depth, substratum and oceanographic stability, whereas environmental variability explained substantially more variation in species richness (40-56%). Two peaks in species richness occurred, the first at 1300-1400 m where cooler Wyville Thomson Overflow Water (WTOW) mixes with subtropical gyre waters and the second at 1500-1600 m where WTOW mixes with subpolar mode waters. Our results suggest that internal tides, substrate heterogeneity and oceanographic interfaces may enhance biological diversity on this and adjacent seamounts in the Rockall Trough.

Fine-scale nutrient and carbonate system dynamics around cold-water coral reefs in the northeast Atlantic.

Ocean acidification has been suggested as a serious threat to the future existence of cold-water corals (CWC). However, there are few fine-scale temporal and spatial datasets of carbonate and nutrients conditions available for these reefs, which can provide a baseline definition of extant conditions. Here we provide observational data from four different sites in the northeast Atlantic that are known habitats for CWC. These habitats differ by depth and by the nature of the coral habitat. At depths where CWC are known to occur across these sites the dissolved inorganic carbon ranged from 2088 to 2186 µmol kg(-1), alkalinity ranged from 2299 to 2346 µmol kg(-1), and aragonite Ω ranged from 1.35 to 2.44. At two sites fine-scale hydrodynamics caused increased variability in the carbonate and nutrient conditions over daily time-scales. The observed high level of variability must be taken into account when assessing CWC sensitivities to future environmental change.

Sensitivity to ocean acidification parallels natural pCO2 gradients experienced by Arctic copepods under winter sea ice.

The Arctic Ocean already experiences areas of low pH and high CO2, and it is expected to be most rapidly affected by future ocean acidification (OA). Copepods comprise the dominant Arctic zooplankton; hence, their responses to OA have important implications for Arctic ecosystems, yet there is little data on their current under-ice winter ecology on which to base future monitoring or make predictions about climate-induced change. Here, we report results from Arctic under-ice investigations of copepod natural distributions associated with late-winter carbonate chemistry environmental data and their response to manipulated pCO2 conditions (OA exposures). Our data reveal that species and life stage sensitivities to manipulated OA conditions were correlated with their vertical migration behavior and with their natural exposures to different pCO2 ranges. Vertically migrating adult Calanus spp. crossed a pCO2 range of >140 µatm daily and showed only minor responses to manipulated high CO2. Oithona similis, which remained in the surface waters and experienced a pCO2 range of <75 µatm, showed significantly reduced adult and nauplii survival in high CO2 experiments. These results support the relatively untested hypothesis that the natural range of pCO2 experienced by an organism determines its sensitivity to future OA and highlight that the globally important copepod species, Oithona spp., may be more sensitive to future high pCO2 conditions compared with the more widely studied larger copepods.

Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification.

Marine pCO2 enrichment via ocean acidification (OA), upwelling and release from carbon capture and storage (CCS) facilities is projected to have devastating impacts on marine biomineralisers and the services they provide. However, empirical studies using stable endpoint pCO2 concentrations find species exhibit variable biological and geochemical responses rather than the expected negative patterns. In addition, the carbonate chemistry of many marine systems is now being observed to be more variable than previously thought. To underpin more robust projections of future OA impacts on marine biomineralisers and their role in ecosystem service provision, we investigate coralline algal responses to realistically variable scenarios of marine pCO2 enrichment. Coralline algae are important in ecosystem function; providing habitats and nursery areas, hosting high biodiversity, stabilizing reef structures and contributing to the carbon cycle. Red coralline marine algae were exposed for 80 days to one of three pH treatments: (i) current pH (control); (ii) low pH (7.7) representing OA change; and (iii) an abrupt drop to low pH (7.7) representing the higher rates of pH change observed at natural vent systems, in areas of upwelling and during CCS releases. We demonstrate that red coralline algae respond differently to the rate and the magnitude of pH change induced by pCO2 enrichment. At low pH, coralline algae survived by increasing their calcification rates. However, when the change to low pH occurred at a fast rate we detected, using Raman spectroscopy, weaknesses in the calcite skeleton, with evidence of dissolution and molecular positional disorder. This suggests that, while coralline algae will continue to calcify, they may be structurally weakened, putting at risk the ecosystem services they provide. Notwithstanding evolutionary adaptation, the ability of coralline algae to cope with OA may thus be determined primarily by the rate, rather than magnitude, at which pCO2 enrichment occurs.

Ocean acidification and rising temperatures may increase biofilm primary productivity but decrease grazer consumption.

Climate change may cause ecosystems to become trophically restructured as a result of primary producers and consumers responding differently to increasing CO2 and temperature. This study used an integrative approach using a controlled microcosm experiment to investigate the combined effects of CO2 and temperature on key components of the intertidal system in the UK, biofilms and their consumers (Littorina littorea). In addition, to identify whether pre-exposure to experimental conditions can alter experimental outcomes we explicitly tested for differential effects on L. littorea pre-exposed to experimental conditions for two weeks and five months. In contrast to predictions based on metabolic theory, the combination of elevated temperature and CO2 over a five-week period caused a decrease in the amount of primary productivity consumed by grazers, while the abundance of biofilms increased. However, long-term pre-exposure to experimental conditions (five months) altered this effect, with grazing rates in these animals being greater than in animals exposed only for two weeks. We suggest that the structure of future ecosystems may not be predictable using short-term laboratory experiments alone owing to potentially confounding effects of exposure time and effects of being held in an artificial environment over prolonged time periods. A combination of laboratory (physiology responses) and large, long-term experiments (ecosystem responses) may therefore be necessary to adequately predict the complex and interactive effects of climate change as organisms may acclimate to conditions over the longer term.

Tidal downwelling and implications for the carbon biogeochemistry of cold-water corals in relation to future ocean acidification and warming.

Cold-water coral (CWC) reefs are recognized as ecologically and biologically significant areas that generate habitats and diversity. The interaction between hydrodynamics and CWCs has been well studied at the Mingulay Reef Complex, a relatively shallow area of reefs found on the continental shelf off Scotland, UK. Within 'Mingulay Area 01' a rapid tidal downwelling of surface waters, brought about as an internal wave, is known to supply warmer, phytoplankton-rich waters to corals growing on the northern flank of an east-west trending seabed ridge. This study shows that this tidal downwelling also causes short-term perturbations in the inorganic carbon (CT ) and nutrient dynamics through the water column and immediately above the reef. Over a 14 h period, corresponding to one semi-diurnal tidal cycle, seawater pH overlying the reef varied by ca. 0.1 pH unit, while pCO2 shifted by >60 µatm, a shift equivalent to a ca. 25 year jump into the future, with respect to atmospheric pCO2 . During the summer stratified period, these downwelling events result in the reef being washed over with surface water that has higher pH, is warmer, nutrient depleted, but rich in phytoplankton-derived particles compared to the deeper waters in which the corals sit. Empirical observations, together with outputs from the European Regional Shelf Sea Ecosystem Model, demonstrate that the variability that the CWC reefs experience changes through the seasons and into the future. Hence, as ocean acidification and warming increase into the future, the downwelling event specific to this site could provide short-term amelioration of corrosive conditions at certain times of the year; however, it could additionally result in enhanced detrimental impacts of warming on CWCs. Natural variability in the CT and nutrient conditions, as well as local hydrodynamic regimes, must be accounted for in any future predictions concerning the responses of marine ecosystems to climate change.

Biological impacts of enhanced alkalinity in Carcinus maenas.

Further steps are needed to establish feasible alleviation strategies that are able to reduce the impacts of ocean acidification, whilst ensuring minimal biological side-effects in the process. Whilst there is a growing body of literature on the biological impacts of many other carbon dioxide reduction techniques, seemingly little is known about enhanced alkalinity. For this reason, we investigated the potential physiological impacts of using chemical sequestration as an alleviation strategy. In a controlled experiment, Carcinus maenas were acutely exposed to concentrations of Ca(OH)2 that would be required to reverse the decline in ocean surface pH and return it to pre-industrial levels. Acute exposure significantly affected all individuals' acid-base balance resulting in slight respiratory alkalosis and hyperkalemia, which was strongest in mature females. Although the trigger for both of these responses is currently unclear, this study has shown that alkalinity addition does alter acid-base balance in this comparatively robust crustacean species.

Effects of elevated CO2 on the reproduction of two calanoid copepods.

Some planktonic groups suffer negative effects from ocean acidification (OA), although copepods might be less sensitive. We investigated the effect of predicted CO2 levels (range 480-750ppm), on egg production and hatching success of two copepod species, Centropages typicus and Temora longicornis. In these short-term incubations there was no significant effect of high CO2 on these parameters. Additionally a very high CO2 treatment, (CO2=9830ppm), representative of carbon capture and storage scenarios, resulted in a reduction of egg production rate and hatching success of C. typicus, but not T. longicornis. In conclusion, reproduction of C. typicus was more sensitive to acute elevated seawater CO2 than that of T. longicornis, but neither species was affected by exposure to CO2 levels predicted for the year 2100. The duration and seasonal timing of exposures to high pCO2, however, might have a significant effect on the reproduction success of calanoid copepods.

Can ocean acidification affect population dynamics of the barnacle Semibalanus balanoides at its southern range edge?

The global ocean and atmosphere are warming. There is increasing evidence suggesting that, in addition to other environmental factors, climate change is affecting species distributions and local population dynamics. Additionally, as a consequence of the growing levels of atmospheric carbon dioxide (CO2), the oceans are taking up increasing amounts of this CO2, causing ocean pH to decrease (ocean acidification). The relative impacts of ocean acidification on population dynamics have yet to be investigated, despite many studies indicating that there will be at least a sublethal impact on many marine organisms, particularly key calcifying organisms. Using empirical data, we forced a barnacle (Semibalanus balanoides) population model to investigate the relative influence of sea surface temperature (SST) and ocean acidification on a population nearing the southern limit of its geographic distribution. Hindcast models were compared to observational data from Cellar Beach (southwestern United Kingdom). Results indicate that a declining pH trend (-0.0017 unit/yr), indicative of ocean acidification over the past 50 years, does not cause an observable impact on the population abundance relative to changes caused by fluctuations in temperature. Below the critical temperature (here T(crit) = 13.1 degrees C), pH has a more significant affect on population dynamics at this southern range edge. However, above this value, SST has the overriding influence. At lower SST, a decrease in pH (according to the National Bureau of Standards, pHNBs) from 8.2 to 7.8 can significantly decrease the population abundance. The lethal impacts of ocean acidification observed in experiments on early life stages reduce cumulative survival by approximately 25%, which again will significantly alter the population level at this southern limit. Furthermore, forecast predictions from this model suggest that combined acidification and warming cause this local population to die out 10 years earlier than would occur if there was only global warming and no concomitant decrease in pH.

Increasing costs due to ocean acidification drives phytoplankton to be more heavily calcified: optimal growth strategy of coccolithophores.

Ocean acidification is potentially one of the greatest threats to marine ecosystems and global carbon cycling. Amongst calcifying organisms, coccolithophores have received special attention because their calcite precipitation plays a significant role in alkalinity flux to the deep ocean (i.e., inorganic carbon pump). Currently, empirical effort is devoted to evaluating the plastic responses to acidification, but evolutionary considerations are missing from this approach. We thus constructed an optimality model to evaluate the evolutionary response of coccolithophorid life history, assuming that their exoskeleton (coccolith) serves to reduce the instantaneous mortality rates. Our model predicted that natural selection favors constructing more heavily calcified exoskeleton in response to increased acidification-driven costs. This counter-intuitive response occurs because the fitness benefit of choosing a better-defended, slower growth strategy in more acidic conditions, outweighs that of accelerating the cell cycle, as this occurs by producing less calcified exoskeleton. Contrary to the widely held belief, the evolutionarily optimized population can precipitate larger amounts of CaCO(3) during the bloom in more acidified seawater, depending on parameter values. These findings suggest that ocean acidification may enhance the calcification rates of marine organisms as an adaptive response, possibly accompanied by higher carbon fixation ability. Our theory also provides a compelling explanation for the multispecific fossil time-series record from ∼200 years ago to present, in which mean coccolith size has increased along with rising atmospheric CO(2) concentration.