Tessa M. Hill

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.

Functional impacts of ocean acidification in an ecologically critical foundation species

SUMMARY Anthropogenic CO2 is reducing the pH and altering the carbonate chemistry of seawater, with repercussions for marine organisms and ecosystems. Current research suggests that calcification will decrease in many species, but compelling evidence of impaired functional performance of calcium carbonate structures is sparse, particularly in key species. Here we demonstrate that ocean acidification markedly degrades the mechanical integrity of larval shells in the mussel Mytilus californianus, a critical community member on rocky shores throughout the northeastern Pacific. Larvae cultured in seawater containing CO2 concentrations expected by the year 2100 (540 or 970 ppm) precipitated weaker, thinner and smaller shells than individuals raised under present-day seawater conditions (380 ppm), and also exhibited lower tissue mass. Under a scenario where mussel larvae exposed to different CO2 levels develop at similar rates, these trends suggest a suite of potential consequences, including an exacerbated vulnerability of new settlers to crushing and drilling attacks by predators; poorer larval condition, causing increased energetic stress during metamorphosis; and greater risks from desiccation at low tide due to shifts in shell area to body mass ratios. Under an alternative scenario where responses derive exclusively from slowed development, with impacted individuals reaching identical milestones in shell strength and size by settlement, a lengthened larval phase could increase exposure to high planktonic mortality rates. In either case, because early life stages operate as population bottlenecks, driving general patterns of distribution and abundance, the ecological success of this vital species may be tied to how ocean acidification proceeds in coming decades.

Foraminifera as indicators of methane-rich environments: A study of modern methane seeps in Santa Barbara Channel, California

Methane hydrates have been implicated as a possible forcing mechanism for rapid climate change during the late Quaternary, via the release of methane from marine reservoirs. Carbon isotopic excursions of foraminifera observed in high-resolution sediment records from Santa Barbara Basin (ODP Site 893) have been interpreted as evidence of episodes of methane release during the late Quaternary. However, the potential relationship between methane in the modern environment and its effect on the stable isotopic composition of benthic and planktonic foraminifera is not well understood. Short cores taken inside a ∼500-m-diameter pockmark with active methane seeps in Santa Barbara Channel, CA, USA, yield information on the effect of high concentrations of environmental methane on foraminiferal assemblages and their stable isotopic composition. These seeps reside at ∼120 m water depth in the eastern portion of the channel, associated with faults and fractures in the Miocene Monterey Formation. Planktonic foraminiferal assemblages and radiocarbon ages show that surface sediments are of late Glacial age (∼25 300 calendar years). This finding suggests an absence of Holocene and deglacial sedimentation in the seep area, likely due the formation of the pockmarks and subsequent winnowing or lack of sedimentation. Benthic foraminiferal assemblages are marked by high abundance of Bolivina tumida, a species previously observed during interstadial episodes and the early Holocene in Santa Barbara Basin, interpreted to include episodes of high methane flux from the basin. While oxygen isotopic values of both benthic and planktonic foraminifera appear normal for cool, glacial conditions, negative carbon isotopic values are seen in benthic foraminifera, primarily in the near-surface intervals. In one interval (1–2 cm below surface), both benthic and planktonic species record highly negative carbon isotopic values, implying that isotopically light methane influenced the entire water column. This spike is of similar or larger magnitude than several earlier observed spikes in the late Quaternary record from ODP Site 893. Single specimen isotopic analyses give an indication of the total range of carbon isotopic values recorded (−0.01 to −25.23‰ for benthics, −0.07 to −22.22‰ for planktonics) in the spike interval. Since modern methane seeps are commonly associated with authigenic carbonate precipitation, scanning electron microscopy was used to assess the possibility that post-depositional alteration may have affected the isotopic composition of the test. These experiments indicate that authigenic carbonate is absent and therefore unable to account for the highly negative carbon isotopic signatures. These data improve our understanding of methane-associated environments by showing that foraminiferal isotopic composition and assemblages may be used to discern the flux of methane from the oceanic reservoir in the geologic record.

Upper-ocean-to-atmosphere radiocarbon offsets imply fast deglacial carbon dioxide release

Radiocarbon in the atmosphere is regulated largely by ocean circulation, which controls the sequestration of carbon dioxide (CO2) in the deep sea through atmosphere–ocean carbon exchange. During the last glaciation, lower atmospheric CO2 levels were accompanied by increased atmospheric radiocarbon concentrations that have been attributed to greater storage of CO2 in a poorly ventilated abyssal ocean. The end of the ice age was marked by a rapid increase in atmospheric CO2 concentrations that coincided with reduced 14C/12C ratios (Δ14C) in the atmosphere, suggesting the release of very ‘old’ (14C-depleted) CO2 from the deep ocean to the atmosphere. Here we present radiocarbon records of surface and intermediate-depth waters from two sediment cores in the southwest Pacific and Southern oceans. We find a steady 170 per mil decrease in Δ14C that precedes and roughly equals in magnitude the decrease in the atmospheric radiocarbon signal during the early stages of the glacial–interglacial climatic transition. The atmospheric decrease in the radiocarbon signal coincides with regionally intensified upwelling and marine biological productivity, suggesting that CO2 released by means of deep water upwelling in the Southern Ocean lost most of its original depleted-14C imprint as a result of exchange and isotopic equilibration with the atmosphere. Our data imply that the deglacial 14C depletion previously identified in the eastern tropical North Pacific must have involved contributions from sources other than the previously suggested carbon release by way of a deep Southern Ocean pathway, and may reflect the expanded influence of the 14C-depleted North Pacific carbon reservoir across this interval. Accordingly, shallow water masses advecting north across the South Pacific in the early deglaciation had little or no residual 14C-depleted signals owing to degassing of CO2 and biological uptake in the Southern Ocean.

Ocean acidification increases the vulnerability of native oysters to predation by invasive snails.

There is growing concern that global environmental change might exacerbate the ecological impacts of invasive species by increasing their per capita effects on native species. However, the mechanisms underlying such shifts in interaction strength are poorly understood. Here, we test whether ocean acidification, driven by elevated seawater pCO2, increases the susceptibility of native Olympia oysters to predation by invasive snails. Oysters raised under elevated pCO2 experienced a 20% increase in drilling predation. When presented alongside control oysters in a choice experiment, 48% more high-CO2 oysters were consumed. The invasive snails were tolerant of elevated CO2 with no change in feeding behaviour. Oysters raised under acidified conditions did not have thinner shells, but were 29–40% smaller than control oysters, and these smaller individuals were consumed at disproportionately greater rates. Reduction in prey size is a common response to environmental stress that may drive increasing per capita effects of stress-tolerant invasive predators.

Paleoceanographic Insights on Recent Oxygen Minimum Zone Expansion: Lessons for Modern Oceanography

Climate-driven Oxygen Minimum Zone (OMZ) expansions in the geologic record provide an opportunity to characterize the spatial and temporal scales of OMZ change. Here we investigate OMZ expansion through the global-scale warming event of the most recent deglaciation (18-11 ka), an event with clear relevance to understanding modern anthropogenic climate change. Deglacial marine sediment records were compiled to quantify the vertical extent, intensity, surface area and volume impingements of hypoxic waters upon continental margins. By integrating sediment records (183-2,309 meters below sea level; mbsl) containing one or more geochemical, sedimentary or microfossil oxygenation proxies integrated with analyses of eustatic sea level rise, we reconstruct the timing, depth and intensity of seafloor hypoxia. The maximum vertical OMZ extent during the deglaciation was variable by region: Subarctic Pacific (~600-2,900 mbsl), California Current (~330-1,500 mbsl), Mexico Margin (~330-830 mbsl), and the Humboldt Current and Equatorial Pacific (~110-3,100 mbsl). The timing of OMZ expansion is regionally coherent but not globally synchronous. Subarctic Pacific and California Current continental margins exhibit tight correlation to the oscillations of Northern Hemisphere deglacial events (Termination IA, Bølling-Allerød, Younger Dryas and Termination IB). Southern regions (Mexico Margin and the Equatorial Pacific and Humboldt Current) exhibit hypoxia expansion prior to Termination IA (~14.7 ka), and no regional oxygenation oscillations. Our analyses provide new evidence for the geographically and vertically extensive expansion of OMZs, and the extreme compression of upper-ocean oxygenated ecosystems during the geologically recent deglaciation.

Climatically driven emissions of hydrocarbons from marine sediments during deglaciation

Marine hydrocarbon seepage emits oil and gas, including methane (≈30 Tg of CH4 per year), to the ocean and atmosphere. Sediments from the California margin contain preserved tar, primarily formed through hydrocarbon weathering at the sea surface. We present a record of variation in the abundance of tar in sediments for the past 32,000 years, providing evidence for increases in hydrocarbon emissions before and during Termination IA [16,000 years ago (16 ka) to 14 ka] and again over Termination IB (11–10 ka). Our study provides direct evidence for increased hydrocarbon seepage associated with deglacial warming through tar abundance in marine sediments, independent of previous geochemical proxies. Climate-sensitive gas hydrates may modulate thermogenic hydrocarbon seepage during deglaciation.

Response of seafloor ecosystems to abrupt global climate change

Significance This investigation presents the first record to our knowledge of the disturbance and recovery of seafloor ecosystem biodiversity in response to abrupt climate change. Ocean sediments have been extensively studied using geochemical and microfaunal (e.g., Foraminifera) analyses; however, these traditional approaches produce limited interpretations of ecological and community-scale responses. We demonstrate here that ocean sediments harbor metazoan fossil material that can be used to reconstruct the response of seafloor biodiversity to global-scale climate events. We show that the last deglaciation, the most recent episode of climate warming, was accompanied by abrupt reorganizations of continental margin seafloor ecosystems through expansions and contractions of the subsurface low-oxygen zones. This archive reveals that global climate change disturbs seafloor ecosystems on continental margins and commits them to millennia of ecological recovery. Anthropogenic climate change is predicted to decrease oceanic oxygen (O2) concentrations, with potentially significant effects on marine ecosystems. Geologically recent episodes of abrupt climatic warming provide opportunities to assess the effects of changing oxygenation on marine communities. Thus far, this knowledge has been largely restricted to investigations using Foraminifera, with little being known about ecosystem-scale responses to abrupt, climate-forced deoxygenation. We here present high-resolution records based on the first comprehensive quantitative analysis, to our knowledge, of changes in marine metazoans (Mollusca, Echinodermata, Arthropoda, and Annelida; >5,400 fossils and trace fossils) in response to the global warming associated with the last glacial to interglacial episode. The molluscan archive is dominated by extremophile taxa, including those containing endosymbiotic sulfur-oxidizing bacteria (Lucinoma aequizonatum) and those that graze on filamentous sulfur-oxidizing benthic bacterial mats (Alia permodesta). This record, from 16,100 to 3,400 y ago, demonstrates that seafloor invertebrate communities are subject to major turnover in response to relatively minor inferred changes in oxygenation (>1.5 to <0.5 mL⋅L−1 [O2]) associated with abrupt (<100 y) warming of the eastern Pacific. The biotic turnover and recovery events within the record expand known rates of marine biological recovery by an order of magnitude, from <100 to >1,000 y, and illustrate the crucial role of climate and oceanographic change in driving long-term successional changes in ocean ecosystems.

Temperature and vital effect controls on bamboo coral (Isididae) isotope geochemistry: A test of the “lines method”

Deep-sea bamboo corals hold promise as long-term climatic archives, yet little information exists linking bamboo coral geochemistry to measured environmental parameters. This study focuses on a suite of 10 bamboo corals collected from the Pacific and Atlantic basins (250–2136 m water depth) to investigate coral longevity, growth rates, and isotopic signatures. Calcite samples for stable isotopes and radiocarbon were collected from the base the corals, where the entire history of growth is recorded. In three of the coral specimens, samples were also taken from an upper branch for comparison. Radiocarbon and growth band width analyses indicate that the skeletal calcite precipitates from ambient dissolved inorganic carbon and that the corals live for 150–300 years, with extension rates of 9–128 μm/yr. A linear relationship between coral calcite δ18O and δ13C indicates that the isotopic composition is influenced by vital effects (δ18O:δ13C slope of 0.17–0.47). As with scleractinian deep-sea corals, the intercept from a linear regression of δ18O versus δ13C is a function of temperature, such that a reliable paleotemperature proxy can be obtained, using the “lines method.” Although the coral calcite δ18O:δ13C slope is maintained throughout the coral base ontogeny, the branches and central cores of the bases exhibit δ18O:δ13C values that are shifted far from equilibrium. We find that a reliable intercept value can be derived from the δ18O:δ13C regression of multiple samples distributed throughout one specimen or from multiple samples within individual growth bands.

Vertical oxygen minimum zone oscillations since 20 ka in Santa Barbara Basin: A benthic foraminiferal community perspective

[1] Here we present a history of deoxygenation of upper intermediate waters during the last deglaciation from Santa Barbara Basin (SBB), based on quantitative analyses of benthic foraminiferal assemblages, from a new shallow piston core above basin sill depth (MV0811-15JC, 418m), and previously described sequences in the deeper basin (MD02-2504, 481m and MD02-2503, 570m). We document a 152m depth transect of benthic foraminiferal assemblages to extract changing community structure (density, diversity, and evenness) and improve paleoenvironmental interpretation of late Quaternary vertical oscillations in the upper boundary of the oxygen minimum zone (OMZ). Close interaction between changes in open margin OMZ and that of the restricted SBB is documented using these quantitative techniques. MV0811-15JC, while being unlaminated, contains strongly hypoxic foraminiferal assemblages (including species Bolivina tumida and Nonionella stella), coeval with preserved sediment laminations in the deeper cores. Last Glacial Maximum (LGM) assemblages across this transect contained oxic fauna and high diversity. At 14.7ka, glacial termination IA, hypoxic benthic fauna appeared across the transect, recording hypoxic waters (<0.5mlL 1 ) <300m from the ocean surface. Bolling/Allerod (B/A) assemblages uniquely stand out in the record, exhibited by low density, diversity, and evenness, and taxonomic composition reflecting extreme and stressful hypoxia and methane-rich environments. Younger Dryas assemblages were diverse and composed of oxic fauna, similar to LGM assemblages. Termination IB initiated another deoxygenation shift, followed by OMZ-associated faunal and density patterns. This analysis strengthens the quantitative assessment of oxygen concentrations involved in deglacial OMZ change and reveals the unexpected, remarkable shallowness of OMZ influence during the B/A.