Natural variation, and the capacity to adapt to ocean acidification in the keystone sea urchin Strongylocentrotus purpuratus

A rapidly growing body of literature documents the potential negative effects of CO₂-driven ocean acidification (OA) on marine organisms. However, nearly all of this work has focused on the effects of future conditions on modern populations, neglecting the role of adaptation. Rapid evolution can alter demographic responses to environmental change, ultimately affecting the likelihood of population persistence, but the capacity for adaptation will differ among populations and species. Here, we measure the capacity of the ecologically important purple sea urchin Strongylocentrotus purpuratus to adapt to OA, using a breeding experiment to estimate additive genetic variance for larval size (an important component of fitness) under future high pCO₂/low pH conditions. Although larvae reared under future conditions were smaller than those reared under present-day conditions, we show that there is also abundant genetic variation for body size under elevated pCO₂, indicating that this trait can evolve. The observed heritability of size was 0.40±0.32 (95% CI) under low pCO₂, and 0.50±0.30 under high pCO₂ conditions. Accounting for the observed genetic variation in models of future larval size and demographic rates substantially alters projections of performance for this species in the future ocean. Importantly, our model shows that after incorporating the effects of adaptation, the OA-driven decrease in population growth rate is up to 50% smaller, than that predicted by the “no-adaptation” scenario. Adults used in the experiment were collected from two sites on the coast of the Northeast Pacific that are characterized by different pH regimes, as measured by autonomous sensors. Comparing results between sites, we also found subtle differences in larval size under high pCO₂ rearing conditions, consistent with local adaptation to carbonate chemistry in the field. These results suggest that spatially varying selection may help to maintain genetic variation necessary for adaptation to future ocean acidification.

Fertilization success of an arctic sea urchin species, Strongylocentrotus droebachiensis (O. F. Müller, 1776) under CO2-induced ocean acidification

Sea urchins as broadcasting spawners, release their gametes into open water for fertilization, thus being particularly vulnerable to ocean acidification. In this study, we assessed the effects of different pH scenarios on fertilization success of Strongylocentrotus droebachiensis, collected at Spitsbergen, Arctic. We achieved acidification by bubbling CO₂ into filtered seawater using partial pressures (pCO₂) of 180, 380, 980, 1400 and 3000 μatm}. Untreated filtered seawater was used as control. We recorded fertilization rates and diagnosed morphological aberrations after post-fertilization periods of 1 h and 3 h under different exposure conditions in experiments with and without pre-incubation of the eggs prior to fertilization. In parallel, we conducted measurements of intracellular pH changes using BCECF/AM in unfertilized eggs exposed to a range of acidified seawater. We observed increasing rates of polyspermy in relation to higher seawater pCO₂, which might be due to failures in the formation of the fertilization envelope. In addition, our experiments showed anomalies in fertilized eggs: incomplete lifting-off of the fertilization envelope and blebs of the hyaline layer. Other drastic malformations consisted of constriction, extrusion, vacuolization or degeneration (observed as a gradient from the cortex to the central region of the cell) of the egg cytoplasm, and irregular cell divisions until 2- to 4-cell stages. The intracellular pH (pH_i) decreased significantly from 1400 μatm on. All results indicate a decreasing fertilization success at CO₂ concentrations from 1400 μatm upwards. Exposure time to low pH might be a threatening factor for the cellular buffer capacity, viability, and development after fertilization.

Long-term trends in calcifying plankton and pH in the North Sea

Relationships between six calcifying plankton groups and pH are explored in a highly biologically productive and data-rich area of the central North Sea using time-series datasets. The long-term trends show that abundances of foraminiferans, coccolithophores, and echinoderm larvae have risen over the last few decades while the abundances of bivalves and pteropods have declined. Despite good coverage of pH data for the study area there is uncertainty over the quality of this historical dataset; pH appears to have been declining since the mid 1990s but there was no statistical connection between the abundance of the calcifying plankton and the pH trends. If there are any effects of pH on calcifying plankton in the North Sea they appear to be masked by the combined effects of other climatic (e.g. temperature), chemical (nutrient concentrations) and biotic (predation) drivers. Certain calcified plankton have proliferated in the central North Sea, and are tolerant of changes in pH that have occurred since the 1950s but bivalve larvae and pteropods have declined. An improved monitoring programme is required as ocean acidification may be occurring at a rate that will exceed the environmental niches of numerous planktonic taxa, testing their capacities for acclimation and genetic adaptation.

Cascading effects of ocean acidification in a rocky subtidal community

Temperate marine rocky habitats may be alternatively characterized by well vegetated macroalgal assemblages or barren grounds, as a consequence of direct and indirect human impacts (e.g. overfishing) and grazing pressure by herbivorous organisms. In future scenarios of ocean acidification, calcifying organisms are expected to be less competitive: among these two key elements of the rocky subtidal food web, coralline algae and sea urchins. In order to highlight how the effects of increased pCO₂ on individual calcifying species will be exacerbated by interactions with other trophic levels, we performed an experiment simultaneously testing ocean acidification effects on primary producers (calcifying and non-calcifying algae) and their grazers (sea urchins). Artificial communities, composed by juveniles of the sea urchin Paracentrotus lividus and calcifying (Corallina elongata) and non-calcifying (Cystoseira amentacea var stricta, Dictyota dichotoma) macroalgae, were subjected to pCO₂ levels of 390, 550, 750 and 1000 µatm in the laboratory. Our study highlighted a direct pCO₂ effect on coralline algae and on sea urchin defense from predation (test robustness). There was no direct effect on the non-calcifying macroalgae. More interestingly, we highlighted diet-mediated effects on test robustness and on the Aristotle’s lantern size. In a future scenario of ocean acidification a decrease of sea urchins’ density is expected, due to lower defense from predation, as a direct consequence of pH decrease, and to a reduced availability of calcifying macroalgae, important component of urchins’ diet. The effects of ocean acidification may therefore be contrasting on well vegetated macroalgal assemblages and barren grounds: in the absence of other human impacts, a decrease of biodiversity can be predicted in vegetated macroalgal assemblages, whereas a lower density of sea urchin could help the recovery of shallow subtidal rocky areas affected by overfishing from barren grounds to assemblages dominated by fleshy macroalgae.

Evolutionary change during experimental ocean acidification

Rising atmospheric carbon dioxide (CO₂) conditions are driving unprecedented changes in seawater chemistry, resulting in reduced pH and carbonate ion concentrations in the Earth’s oceans. This ocean acidification has negative but variable impacts on individual performance in many marine species. However, little is known about the adaptive capacity of species to respond to an acidified ocean, and, as a result, predictions regarding future ecosystem responses remain incomplete. Here we demonstrate that ocean acidification generates striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus) cultured under different CO₂ levels. We examined genetic change at 19,493 loci in larvae from seven adult populations cultured under realistic future CO₂ levels. Although larval development and morphology showed little response to elevated CO₂, we found substantial allelic change in 40 functional classes of proteins involving hundreds of loci. Pronounced genetic changes, including excess amino acid replacements, were detected in all populations and occurred in genes for biomineralization, lipid metabolism, and ion homeostasis—gene classes that build skeletons and interact in pH regulation. Such genetic change represents a neglected and important impact of ocean acidification that may influence populations that show few outward signs of response to acidification. Our results demonstrate the capacity for rapid evolution in the face of ocean acidification and show that standing genetic variation could be a reservoir of resilience to climate change in this coastal upwelling ecosystem. However, effective response to strong natural selection demands large population sizes and may be limited in species impacted by other environmental stressors.

Temperature and CO2 additively regulate physiology, morphology and genomic responses of larval sea urchins, Strongylocentrotus purpuratus

Ocean warming and ocean acidification, both consequences of anthropogenic production of CO₂, will combine to influence the physiological performance of many species in the marine environment. In this study, we used an integrative approach to forecast the impact of future ocean conditions on larval purple sea urchins (Strongylocentrotus purpuratus) from the northeast Pacific Ocean. In laboratory experiments that simulated ocean warming and ocean acidification, we examined larval development, skeletal growth, metabolism and patterns of gene expression using an orthogonal comparison of two temperature (13°C and 18°C) and pCO₂ (400 and 1100 μatm) conditions. Simultaneous exposure to increased temperature and pCO₂ significantly reduced larval metabolism and triggered a widespread downregulation of histone encoding genes. pCO₂ but not temperature impaired skeletal growth and reduced the expression of a major spicule matrix protein, suggesting that skeletal growth will not be further inhibited by ocean warming. Importantly, shifts in skeletal growth were not associated with developmental delay. Collectively, our results indicate that global change variables will have additive effects that exceed thresholds for optimized physiological performance in this keystone marine species.

The response of abyssal organisms to low pH conditions during a series of CO2-release experiments simulating deep-sea carbon sequestration

The effects of low-pH, high-pCO₂ conditions on deep-sea organisms were examined during four deep-sea CO₂ release experiments simulating deep-ocean C sequestration by the direct injection of CO₂ into the deep sea. We examined the survival of common deep-sea, benthic organisms (microbes; macrofauna, dominated by Polychaeta, Nematoda, Crustacea, Mollusca; megafauna, Echinodermata, Mollusca, Pisces) exposed to low-pH waters emanating as a dissolution plume from pools of liquid carbon dioxide released on the seabed during four abyssal CO₂-release experiments. Microbial abundance in deep-sea sediments was unchanged in one experiment, but increased under environmental hypercapnia during another, where the microbial assemblage may have benefited indirectly from the negative impact of low-pH conditions on other taxa. Lower abyssal metazoans exhibited low survival rates near CO₂ pools. No urchins or holothurians survived during 30–42 days of exposure to episodic, but severe environmental hypercapnia during one experiment (E1; pH reduced by as much as ca. 1.4 units). These large pH reductions also caused 75% mortality for the deep-sea amphipod, Haploops lodo, near CO₂ pools. Survival under smaller pH reductions (ΔpH<0.4 units) in other experiments (E2, E3, E5) was higher for all taxa, including echinoderms. Cephalopods, gastropods, and fish were more tolerant than most other taxa. The gastropod Mohnia vernalis and octopus Benthoctopus sp. survived exposure to pH reductions that episodically reached −0.3 pH units. Ninety percent of abyssal zoarcids (Pachycara bulbiceps) survived exposure to pH changes reaching ca. −0.3 pH units during 30–42 day-long experiments.

Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming

Ocean acidification and warming are considered two of the greatest threats to marine biodiversity, yet the combined effect of these stressors on marine organisms remains largely unclear. Using a meta-analytical approach, we assessed the biological responses of marine organisms to the effects of ocean acidification and warming in isolation and combination. As expected biological responses varied across taxonomic groups, life-history stages, and trophic levels, but importantly, combining stressors generally exhibited a stronger biological (either positive or negative) effect. Using a subset of orthogonal studies, we show that four of five of the biological responses measured (calcification, photosynthesis, reproduction, and survival, but not growth) interacted synergistically when warming and acidification were combined. The observed synergisms between interacting stressors suggest that care must be made in making inferences from single-stressor studies. Our findings clearly have implications for the development of adaptive management strategies particularly given that the frequency of stressors interacting in marine systems will be likely to intensify in the future. There is now an urgent need to move toward more robust, holistic, and ecologically realistic climate change experiments that incorporate interactions. Without them accurate predictions about the likely deleterious impacts to marine biodiversity and ecosystem functioning over the next century will not be possible.

Consequences of ocean change for ecological function: observational and modeling case studies of larval echinoderms

Planktonic larvae of many marine invertebrates play important roles in connecting and sustaining disjunct adult populations. Most larvae are denser than seawater and rely on swimming to regulate their vertical positions. Because environmental variables including direction and strength of advective currents and prey and predator concentrations vary with depth, larval swimming behaviors can significantly impact larval survival and transport. Quantification of larval movement is therefore essential for understanding population dynamics, especially in the face of global climate change because of the need to predict possible shifts in ecosystems. Larval swimming is physically constrained by their morphologies, which are often complex and highly variable. Behavioral responses to surrounding environmental variables modulate the actual swimming performance within physical limits. This study took a two-pronged approach to understand larval swimming through 1) quantifying larval behaviors under changing environmental conditions and 2) modeling larval morphology-flow interactions. This study applied novel non-invasive video motion analysis techniques to quantify effects of environmental variations. Ocean acidification is considered one of the major threats to marine ecosystems and larvae are suggested to be particularly vulnerable. When reared under elevated pCO2 level, larval sand dollars Dendraster excentricus maintained their swimming performance but had lower feeding success. By combining feeding and respiration experiments with motion analysis, we observed similar tradeoffs among larval purple urchins, Strongylocentrotus purpuratus, and heart urchins, Brissopsis lyrifera. These two echinoids also underwent budding under acidified conditions, an asexual reproduction strategy that has not been previously reported. These results suggest that sublethal OA impacts could be carried over from planktonic stages to later development stages and affect population dynamics. Previous studies suggest that larval swimming performance peaks within a tight morphospace. Larval sand dollars are phenotypically plastic and develop longer arms when starved. Starved individuals swam with higher oscillatory speeds than their fed counterpart. To distinguish the biomechanical constraints associated with morphological changes from behavioral adjustments, we developed a detailed 3-dimensional model of individual larvae using laser confocal microscopy and finite-element mesh generation. This novel modeling approach can easily be adapted for other taxa to help understand constraints that swimming imposes on the evolution of larval form.

Vulnerability of the calcifying larval stage of the Antarctic sea urchin Sterechinus neumayeri to near-future ocean acidification and warming

Stenothermal polar benthic marine invertebrates are highly sensitive to environmental perturbations but little is known about potential synergistic effects of concurrent ocean warming and acidification on development of their embryos and larvae. We examined the effects of these stressors on development to the calcifying larval stage in the Antarctic sea urchin Sterechinus neumayeri in embryos reared in present and future (2100+) ocean conditions from fertilization. Embryos were reared in 2 temperature (ambient: -1.0°C, + 2°C: 1.0°C) and 3 pH (ambient: pH 8.0, – 0.2-0.4 pH units: 7.8,7.6) levels. Principle coordinates analysis on five larval metrics showed a significant effect of temperature and pH on the pattern of growth. Within each temperature, larvae were separated by pH treatment, a pattern primarily influenced by larval arm and body length. Growth was accelerated by temperature with a 20-28% increase in postoral (PO) length at +2°C across all pH levels. Growth was strongly depressed by reduced pH with a 8-19% decrease in PO length at pH 7.6-7.8 at both temperatures. The boost in growth caused by warming resulted in larvae that were larger than would be observed if acidification was examined in the absence of warming. However, there was no significant interaction between these stressors. The increase in left-right asymmetry and altered body allometry indicated that decreased pH disrupted developmental patterning and acted as a teratogen (agent causing developmental malformation). Decreased developmental success with just a 2°C warming indicates that development in S. neumayeri is particularly sensitive to increased temperature. Increased temperature also altered larval allometry. Altered body shape impairs swimming and feeding in echinoplutei. In the absence of adaptation, it appears that the larval phase may be a bottleneck for survivorship of S. neumayeri in a changing ocean in a location where poleward migration to escape inhospitable conditions is not possible.