Christina A. Frieder

Oxygen, ecology, and the Cambrian radiation of animals

The Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event and the evident increase in diversity and disparity. Ecological triggers focused on escalatory predator–prey “arms races” can explain the evolutionary pattern but not its timing, whereas environmental triggers, particularly ocean/atmosphere oxygenation, do the reverse. Using modern oxygen minimum zones as an analog for Proterozoic oceans, we explore the effect of low oxygen levels on the feeding ecology of polychaetes, the dominant macrofaunal animals in deep-sea sediments. Here we show that low oxygen is clearly linked to low proportions of carnivores in a community and low diversity of carnivorous taxa, whereas higher oxygen levels support more complex food webs. The recognition of a physiological control on carnivory therefore links environmental triggers and ecological drivers, providing an integrated explanation for both the pattern and timing of Cambrian animal radiation.

Detecting the Unexpected: A Research Framework for Ocean Acidification

The threat that ocean acidification (OA) poses to marine ecosystems is now recognized and U.S. funding agencies have designated specific funding for the study of OA. We present a research framework for studying OA that describes it as a biogeochemical event that impacts individual species and ecosystems in potentially unexpected ways. We draw upon specific lessons learned about ecosystem responses from research on acid rain, carbon dioxide enrichment in terrestrial plant communities, and nitrogen deposition. We further characterize the links between carbon chemistry changes and effects on individuals and ecosystems, and enumerate key hypotheses for testing. Finally, we quantify how U.S. research funding has been distributed among these linkages, concluding that there is an urgent need for research programs designed to anticipate how the effects of OA will reverberate throughout assemblages of species.

Seasonal advection of Pacific Equatorial Water alters oxygen and pH in the Southern California Bight

Chemical properties of the California Undercurrent (CU) have been changing over the past several decades, yet the mechanisms responsible for the trend are still not fully understood. We present a survey of temperature, salinity, O2, pH, and currents at intermediate depths (defined here as 50–500 m) in the summer (30 June to 10 July) and winter (8–15 December) of 2012 in the southern region of the Southern California Bight. Observations of temperature, salinity, and currents reveal that local bathymetry and small gyres play an important role in the flow path of the California Undercurrent (CU). Using spiciness (π) as a tracer, we observe a 10% increase of Pacific Equatorial Water (PEW) in the core of the CU during the summer versus the winter. This is associated with an increase in π of 0.2, and a decrease in O2 and pH of 30 μmol kg−1 and 0.022, respectively; the change in pH is driven by increased CO2, while total alkalinity remains unchanged. The high-π, low-O2, and low-pH waters during the summer are not distributed uniformly in the study region. Moreover, mooring observations at the edge of the continental shelf reveal intermittent intrusions of PEW onto the shelf with concomitant decreases in O2 and pH. We estimate that increased advection of PEW in the CU could account for approximately 50% of the observed decrease in O2, and between 49 and 73% of the decrease in pH, over the past three decades.

Metabolic cost of calcification in bivalve larvae under experimental ocean acidification

&NA; Physiological increases in energy expenditure frequently occur in response to environmental stress. Although energy limitation is often invoked as a basis for decreased calcification under ocean acidification, energy‐relevant measurements related to this process are scant. In this study we focus on first‐shell (prodissoconch I) formation in larvae of the Pacific oyster, Crassostrea gigas. The energy cost of calcification was empirically derived to be ≤ 1.1 &mgr;J (ng CaCO3)−1. Regardless of the saturation state of aragonite (2.77 vs. 0.77), larvae utilize the same amount of total energy to complete first‐shell formation. Even though there was a 56% reduction of shell mass and an increase in dissolution at aragonite undersaturation, first‐shell formation is not energy limited because sufficient endogenous reserves are available to meet metabolic demand. Further studies were undertaken on larvae from genetic crosses of pedigreed lines to test for variance in response to aragonite undersaturation. Larval families show variation in response to ocean acidification, with loss of shell size ranging from no effect to 28%. These differences show that resilience to ocean acidification may exist among genotypes. Combined studies of bioenergetics and genetics are promising approaches for understanding climate change impacts on marine organisms that undergo calcification.

Uranium in larval shells as a barometer of molluscan ocean acidification exposure.

As the ocean undergoes acidification, marine organisms will become increasingly exposed to reduced pH, yet variability in many coastal settings complicates our ability to accurately estimate pH exposure for those organisms that are difficult to track. Here we present shell-based geochemical proxies that reflect pH exposure from laboratory and field settings in larvae of the mussels Mytilus californianus and M. galloprovincialis. Laboratory-based proxies were generated from shells precipitated at pH 7.51 to 8.04. U/Ca, Sr/Ca, and multielemental signatures represented as principal components varied with pH for both species. Of these, U/Ca was the best predictor of pH and did not vary with larval size, with semidiurnal pH fluctuations, or with oxygen concentration. Field applications of U/Ca were tested with mussel larvae reared in situ at both known and unknown pH conditions. Larval shells precipitated in a region of greater upwelling had higher U/Ca, and these U/Ca values corresponded well with the laboratory-derived U/Ca-pH proxy. Retention of the larval shell after settlement in molluscs allows use of this geochemical proxy to assess ocean acidification effects on marine populations.

Transpressional segment boundaries in strike‐slip fault systems offshore southern California: Implications for fluid expulsion and cold seep habitats

The importance of tectonics and fluid flow in controlling cold seep habitats has long been appreciated at convergent margins but remains poorly understood in strike-slip systems. Here we present geophysical, geochemical, and biological data from an active methane seep offshore from Del Mar, California, in the inner California borderlands (ICB). The location of this seep appears controlled by localized transpression associated with a step in the San Diego Trough fault zone and provides an opportunity to examine the interplay between fluid expulsion and restraining step overs along strike-slip fault systems. These segment boundaries may have important controls on seep locations in the ICB and other margins characterized by strike-slip faulting (e.g., Greece, Sea of Marmara, and Caribbean). The strike-slip fault systems offshore southern California appear to have a limited distribution of seep sites compared to a wider distribution at convergent plate boundaries, which may influence seep habitat diversity and connectivity.

Shifting Balance of Protein Synthesis and Degradation Sets a Threshold for Larval Growth Under Environmental Stress

Exogenous environmental factors alter growth rates, yet information remains scant on the biochemical mechanisms and energy trade-offs that underlie variability in the growth of marine invertebrates. Here we study the biochemical bases for differential growth and energy utilization (as adenosine triphosphate [ATP] equivalents) during larval growth of the bivalve Crassostrea gigas exposed to increasing levels of experimental ocean acidification (control, middle, and high pCO2, corresponding to ∼400, ∼800, and ∼1100 µatm, respectively). Elevated pCO2 hindered larval ability to accrete both shell and whole-body protein content. This negative impact was not due to an inability to synthesize protein per se, because size-specific rates of protein synthesis were upregulated at both middle and high pCO2 treatments by as much as 45% relative to control pCO2. Rather, protein degradation rates increased with increasing pCO2. At control pCO2, 89% of cellular energy (ATP equivalents) utilization was accounted for by just 2 processes in larvae, with protein synthesis accounting for 66% and sodium-potassium transport accounting for 23%. The energetic demand necessitated by elevated protein synthesis rates could be accommodated either by reallocating available energy from within the existing ATP pool or by increasing the production of total ATP. The former strategy was observed at middle pCO2, while the latter strategy was observed at high pCO2. Increased pCO2 also altered sodium-potassium transport, but with minimal impact on rates of ATP utilization relative to the impact observed for protein synthesis. Quantifying the actual energy costs and trade-offs for maintaining physiological homeostasis in response to stress will help to reveal the mechanisms of resilience thresholds to environmental change.