Sea butterflies in a pickle: reliable biomarkers and seasonal sensitivity of Limacina retroversa to ocean acidification in the Gulf of Maine.

The passive dissolution of anthropogenically produced CO2 into the ocean system is reducing ocean pH and changing a suite of chemical equilibria, with negative consequences for some marine organisms, in particular those that bear calcium carbonate shells. Although our monitoring of these chemical changes has improved, we have not developed effective tools to translate observations, which are typically of the pH and carbonate saturation state, into ecologically relevant predictions of biological risks. One potential solution is to develop bioindicators: biological variables with a clear relationship to environmental risk factors that can be used for assessment and management. Thecosomatous pteropods are a group of pelagic shelled marine gastropods, whose biological responses to CO2 have been suggested as potential bioindicators of ocean acidification owing to their sensitivity to acidification in both the laboratory and the natural environment. Using five CO2 exposure experiments, occurring across four seasons and running for up to 15 days, we describe a consistent relationship between saturation state, shell transparency and duration of exposure, as well as identify a suite of genes that could be used for biological monitoring with further study. We clarify variations in thecosome responses due to seasonality, resolving prior uncertainties and demonstrating the range of their phenotypic plasticity. These biomarkers of acidification stress can be implemented into ecosystem models and monitoring programmes in regions where pteropods are found, whilst the approach will serve as an example for other regions on how to bridge the gap between point-based chemical monitoring and biologically relevant assessments of ecosystem health.

Mesoscale eddies influence the movements of mature female white sharks in the Gulf Stream and Sargasso Sea.

Satellite-tracking of mature white sharks (Carcharodon carcharias) has revealed open-ocean movements spanning months and covering tens of thousands of kilometers. But how are the energetic demands of these active apex predators met as they leave coastal areas with relatively high prey abundance to swim across the open ocean through waters often characterized as biological deserts? Here we investigate mesoscale oceanographic variability encountered by two white sharks as they moved through the Gulf Stream region and Sargasso Sea in the North Atlantic Ocean. In the vicinity of the Gulf Stream, the two mature female white sharks exhibited extensive use of the interiors of clockwise-rotating anticyclonic eddies, characterized by positive (warm) temperature anomalies. One tagged white shark was also equipped with an archival tag that indicated this individual made frequent dives to nearly 1,000 m in anticyclones, where it was presumably foraging on mesopelagic prey. We propose that warm temperature anomalies in anticyclones make prey more accessible and energetically profitable to adult white sharks in the Gulf Stream region by reducing the physiological costs of thermoregulation in cold water. The results presented here provide valuable new insight into open ocean habitat use by mature, female white sharks that may be applicable to other large pelagic predators.

Exposure to CO2 influences metabolism, calcification and gene expression of the thecosome pteropod Limacina retroversa.

Thecosomatous pteropods, a group of aragonite shell-bearing zooplankton, are becoming an important sentinel organism for understanding the influence of ocean acidification on pelagic organisms. These animals show vulnerability to changing carbonate chemistry conditions, are geographically widespread, and are both biogeochemically and trophically important. The objective of this study was to determine how increasing duration and severity of CO2 treatment influence the physiology of the thecosome Limacina retroversa, integrating both gene expression and organism-level (respiration and calcification) metrics. We exposed pteropods to over-saturated, near-saturated or under-saturated conditions and sampled individuals at 1, 3, 7, 14 and 21 days of exposure to test for the effect of duration. We found that calcification was affected by borderline and under-saturated conditions by week two, while respiration appeared to be more strongly influenced by an interaction between severity and duration of exposure, showing complex changes by one week of exposure. The organismal metrics were corroborated by specific gene expression responses, with increased expression of biomineralization-associated genes in the medium and high treatments throughout and complex changes in metabolic genes corresponding to both captivity and CO2 treatment. Genes associated with other physiological processes such as lipid metabolism, neural function and ion pumping had complex responses, influenced by both duration and severity. Beyond these responses, our findings detail the captivity effects for these pelagic organisms, providing information to contextualize the conclusions of previous studies, and emphasizing a need for better culturing protocols.

Estimation of biological parameters of marine organisms using linear and nonlinear acoustic scattering model-based inversion methods.

The linear inversion commonly used in fisheries and zooplankton acoustics assumes a constant inversion kernel and ignores the uncertainties associated with the shape and behavior of the scattering targets, as well as other relevant animal parameters. Here, errors of the linear inversion due to uncertainty associated with the inversion kernel are quantified. A scattering model-based nonlinear inversion method is presented that takes into account the nonlinearity of the inverse problem and is able to estimate simultaneously animal abundance and the parameters associated with the scattering model inherent to the kernel. It uses sophisticated scattering models to estimate first, the abundance, and second, the relevant shape and behavioral parameters of the target organisms. Numerical simulations demonstrate that the abundance, size, and behavior (tilt angle) parameters of marine animals (fish or zooplankton) can be accurately inferred from the inversion by using multi-frequency acoustic data. The influence of the singularity and uncertainty in the inversion kernel on the inversion results can be mitigated by examining the singular values for linear inverse problems and employing a non-linear inversion involving a scattering model-based kernel.

Ecological Insights from Pelagic Habitats Acquired Using Active Acoustic Techniques.

Marine pelagic ecosystems present fascinating opportunities for ecological investigation but pose important methodological challenges for sampling. Active acoustic techniques involve producing sound and receiving signals from organisms and other water column sources, offering the benefit of high spatial and temporal resolution and, via integration into different platforms, the ability to make measurements spanning a range of spatial and temporal scales. As a consequence, a variety of questions concerning the ecology of pelagic systems lend themselves to active acoustics, ranging from organism-level investigations and physiological responses to the environment to ecosystem-level studies and climate. As technologies and data analysis methods have matured, the use of acoustics in ecological studies has grown rapidly. We explore the continued role of active acoustics in addressing questions concerning life in the ocean, highlight creative applications to key ecological themes ranging from physiology and behavior to biogeography and climate, and discuss emerging avenues where acoustics can help determine how pelagic ecosystems function.

Transcriptome-wide analysis of the response of the thecosome pteropod Clio pyramidata to short-term CO2 exposure.

Thecosome pteropods, a group of calcifying holoplanktonic mollusks, have recently become a research focus due to their potential sensitivity to increased levels of anthropogenic dissolved CO2 in seawater and the accompanying ocean acidification. Some populations, however, already experience high CO2 in their natural distribution during diel vertical migrations. To achieve a better understanding of the mechanisms of pteropod calcification and physiological response to this sort of short duration CO2 exposure, we characterized the gene complement of Clio pyramidata, a cosmopolitan diel migratory thecosome, and investigated its transcriptomic response to experimentally manipulated CO2 conditions. Individuals were sampled from the Northwest Atlantic in the fall of 2011 and exposed to ambient conditions (~380ppm) and elevated CO2 (~800ppm, similar to levels experienced during a diel vertical migration) for ~10h. Following this exposure the respiration rate of the individuals was measured. We then performed RNA-seq analysis, assembled the C. pyramidata transcriptome de novo, annotated the genes, and assessed the differential gene expression patterns in response to exposure to elevated CO2. Within the transcriptome, we identified homologs of genes with known roles in biomineralization in other mollusks, including perlucin, calmodulin, dermatopontin, calponin, and chitin synthases. Respiration rate was not affected by short-term exposure to CO2. Gene expression varied greatly among individuals, and comparison between treatments indicated that C. pyramidata down-regulated a small number of genes associated with aerobic metabolism and up-regulated genes that may be associated with biomineralization, particularly collagens and C-type lectins. These results provide initial insight into the effects of short term CO2 exposure on these important planktonic open-ocean calcifiers, pairing respiration rate and the gene expression level of response, and reveal candidate genes for future ecophysiological, biomaterial and phylogenetic studies.

Reexamination of the species assignment of Diacavolinia pteropods using DNA barcoding.

Thecosome pteropods (Mollusca, Gastropoda) are an ecologically important, diverse, and ubiquitous group of holoplanktonic animals that are the focus of intense research interest due to their external aragonite shell and vulnerability to ocean acidification. Characterizing the response of these animals to low pH and other environmental stressors has been hampered by continued uncertainty in their taxonomic identification. An example of this confusion in species assignment is found in the genus Diacavolinia. All members of this genus were originally indentified as a single species, Cavolinia longirostris, but over the past fifty years the taxonomy has been revisited multiple times; currently the genus comprises 22 different species. This study examines five species of Diacavolinia, including four sampled in the Northeast Atlantic (78 individuals) and one from the Eastern tropical North Pacific (15 individuals). Diacavolina were identified to species based on morphological characteristics according to the current taxonomy, photographed, and then used to determine the sequence of the "DNA barcoding" region of the cytochrome c oxidase subunit I (COI). Specimens from the Atlantic, despite distinct differences in shell morphology, showed polyphyly and a genetic divergence of <3% (K2P distance) whereas the Pacific and Atlantic samples were more distant (≈ 19%). Comparisons of Diacavolinia spp. with other Cavolinia spp. reveal larger distances (≈ 24%). These results indicate that specimens from the Atlantic comprise a single monophyletic species and suggest possible species-level divergence between Atlantic and Pacific populations. The findings support the maintenance of Diacavolinia as a separate genus, yet emphasize the inadequacy of our current taxonomic understanding of pteropods. They highlight the need for accurate species identifications to support estimates of biodiversity, range extent and natural exposure of these planktonic calcifiers to environmental variability; furthermore, the apparent variation of the pteropods shell may have implications for our understanding of the species' sensitivity to ocean acidification.

Atlantic bluefin tuna: a novel multistock spatial model for assessing population biomass.

Atlantic bluefin tuna (Thunnus thynnus) is considered to be overfished, but the status of its populations has been debated, partly because of uncertainties regarding the effects of mixing on fishing grounds. A better understanding of spatial structure and mixing may help fisheries managers to successfully rebuild populations to sustainable levels while maximizing catches. We formulate a new seasonally and spatially explicit fisheries model that is fitted to conventional and electronic tag data, historic catch-at-age reconstructions, and otolith microchemistry stock-composition data to improve the capacity to assess past, current, and future population sizes of Atlantic bluefin tuna. We apply the model to estimate spatial and temporal mixing of the eastern (Mediterranean) and western (Gulf of Mexico) populations, and to reconstruct abundances from 1950 to 2008. We show that western and eastern populations have been reduced to 17% and 33%, respectively, of 1950 spawning stock biomass levels. Overfishing to below the biomass that produces maximum sustainable yield occurred in the 1960s and the late 1990s for western and eastern populations, respectively. The model predicts that mixing depends on season, ontogeny, and location, and is highest in the western Atlantic. Assuming that future catches are zero, western and eastern populations are predicted to recover to levels at maximum sustainable yield by 2025 and 2015, respectively. However, the western population will not recover with catches of 1750 and 12,900 tonnes (the "rebuilding quotas") in the western and eastern Atlantic, respectively, with or without closures in the Gulf of Mexico. If future catches are double the rebuilding quotas, then rebuilding of both populations will be compromised. If fishing were to continue in the eastern Atlantic at the unregulated levels of 2007, both stocks would continue to decline. Since populations mix on North Atlantic foraging grounds, successful rebuilding policies will benefit from trans-Atlantic cooperation.

Determining dominant scatterers of sound in mixed zooplankton populations.

High-frequency acoustic scattering techniques have been used to investigate dominant scatterers in mixed zooplankton populations. Volume backscattering was measured in the Gulf of Maine at 43, 120, 200, and 420 kHz. Zooplankton composition and size were determined using net and video sampling techniques, and water properties were determined using conductivity, temperature, and depth sensors. Dominant scatterers have been identified using recently developed scattering models for zooplankton and microstructure. Microstructure generally did not contribute to the scattering. At certain locations, gas-bearing zooplankton, that account for a small fraction of the total abundance and biomass, dominated the scattering at all frequencies. At these locations, acoustically inferred size agreed well with size determined from the net samples. Significant differences between the acoustic, net, and video estimates of abundance for these zooplankton are most likely due to limitations of the net and video techniques. No other type of biological scatterer ever dominated the scattering at all frequencies. Copepods, fluid-like zooplankton that account for most of the abundance and biomass, dominated at select locations only at the highest frequencies. At these locations, acoustically inferred abundance agreed well with net and video estimates. A general approach for the difficult problem of interpreting high-frequency acoustic scattering in mixed zooplankton populations is described.

Improved parameterization of Antarctic krill target strength models.

There are historical discrepancies between empirical observations of Antarctic krill target strength and predictions using theoretical scattering models. These differences are addressed through improved understanding of key model parameters. The scattering process was modeled using the distorted-wave Born approximation, representing the shape of the animal as a bent and tapered cylinder. Recently published length-based regressions were used to constrain the sound speed and density contrasts between the animal and the surrounding seawater, rather than the earlier approach of using single values for all lengths. To constrain the parameter governing the orientation of the animal relative to the incident acoustic wave, direct measurements of the orientation of krill in situ were made with a video plankton recorder. In contrast to previous indirect and aquarium-based observations, krill were observed to orient themselves mostly horizontally. Averaging predicted scattering over the measured distribution of orientations resulted in predictions of target strength consistent with in situ measurements of target strength of large krill (mean length 40-43 mm) at four frequencies (43-420 kHz), but smaller than expected under the semi-empirical model traditionally used to estimate krill target strength.