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  • 11
    Publication Date: 2021-01-08
    Description: Natural cycles in the seawater partial pressure of carbon dioxide (CO2) in the Gulf of Maine, which vary in surface waters from ~250 to 550 µatm seasonally, provide an opportunity to observe how the life cycle and phenology of the shelled pteropod Limacina retroversa responds to changing food, temperature and carbonate chemistry conditions. Distributional, hydrographic, and physiological sampling suggest that pteropod populations are located in the upper portion of the water column (0–150 m) with a maximum abundance above 50 m. Gene expression and shell condition measurements show that the population already experiences biomineralization stress in the winter months when measured aragonite saturation state was at a seasonal low (though slightly oversaturated), reinforcing the usefulness of this organism as a bio-indicator for pelagic ecosystem response to ocean acidification. There appear to be two reproductive events per year with one pulse timed to coincide with the spring bloom, the period with highest respiration rate, fluorescence, and pH, and a second more extended pulse in the late summer and fall when saturation states remain high and fluorescence begins to decline. During the fall there is transcriptomic evidence of lipid storage for overwintering, allowing the second generation to survive the period of low food and aragonite saturation state. Based on these observations we predict that in the future pteropods will likely be most vulnerable to changing CO2 regionally during the fall reproductive event when CO2 concentration already naturally rises and when there is the added stress of generating lipid stores.
    Type: Article , PeerReviewed
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  • 12
    Publication Date: 2022-01-31
    Description: Interpreting the vulnerability of pelagic calcifiers to ocean acidification (OA) is enhanced by an understanding of their critical thresholds and how these thresholds are modified by other climate change stressors (e.g., warming). To address this need, we undertook a three-part data synthesis for pteropods, one of the calcifying zooplankton group. We conducted the first meta-analysis and threshold analysis of literature characterizing pteropod responses to OA and warming by synthetizing dataset comprising of 2,097 datapoints. Meta-analysis revealed the extent to which responses among studies conducted on differing life stages and disparate geographies could be integrated into a common analysis. The results demonstrated reduced calcification, growth, development, and survival to OA with increased magnitude of sensitivity in the early life stages, under prolonged duration, and with the concurrent exposure of OA and warming, but not species-specific sensitivity. Second, breakpoint analyses identified OA thresholds for several endpoints: dissolution (mild and severe), calcification, egg development, shell growth, and survival. Finally, consensus by a panel of pteropod experts was used to verify thresholds and assign confidence scores for five endpoints with a sufficient signal: noise ratio to develop life-stage specific, duration-dependent thresholds. The range of aragonite saturation state from 1.5–0.9 provides a risk range from early warning to lethal impacts, thus providing a rigorous basis for vulnerability assessments to guide climate change management responses, including an evaluation of the efficacy of local pollution management. In addition, meta-analyses with OA, and warming shows increased vulnerability in two pteropod processes, i.e., shell dissolution and survival, and thus pointing toward increased threshold sensitivity under combined stressor effect.
    Type: Article , PeerReviewed
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  • 13
    Publication Date: 2017-01-10
    Description: The widespread distribution of pteropods, their role in ocean food webs and their sensitivity to ocean acidification and warming has renewed scientific interest in this group of zooplankton. Unfortunately, their fragile shell, sensitivity to handling, unknowns surrounding buoyancy regulation and poorly described feeding mechanisms make thecosome pteropods notoriously difficult to maintain in the laboratory. The resultant high mortality rates and unnatural behaviours may confound experimental findings. The high mortality rate also discourages the use of periods of acclimation to experimental conditions and precludes vital long-term studies. Here we summarize the current status of culture methodology to provide a comprehensive basis for future experimental work and culture system development.
    Repository Name: EPIC Alfred Wegener Institut
    Type: Article , isiRev , info:eu-repo/semantics/article
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  • 14
    Publication Date: 2017-05-04
    Description: The impact of anthropogenic ocean acidification (OA) on marine ecosystems is a vital concern facing marine scientists and managers of ocean resources. Euthecosomatous pteropods (holoplanktonic gastropods) represent an excellent sentinel for indicating exposure to anthropogenic OA because of the sensitivity of their aragonite shells to the OA conditions less favorable for calcification. However, an integration of observations, experiments and modelling efforts is needed to make accurate predictions of how these organisms will respond to future changes to their environment. Our understanding of the underlying organismal biology and life history is far from complete and must be improved if we are to comprehend fully the responses of these organisms to the multitude of stressors in their environment beyond OA. This review considers the present state of research and understanding of euthecosomatous pteropod biology and ecology of these organisms and considers promising new laboratory methods, advances in instrumentation (such as molecular, trace elements, stable isotopes, palaeobiology alongside autonomous sampling platforms, CT scanning and high-quality video recording) and novel field-based approaches (i.e. studies of upwelling and CO2 vent regions) that may allow us to improve our predictive capacity of their vulnerability and/or resilience. In addition to playing a critical ecological and biogeochemical role, pteropods can offer a significant value as an early-indicator of anthropogenic OA. This role as a sentinel species should be developed further to onsolidate their potential use within marine environmental management policy making.
    Repository Name: EPIC Alfred Wegener Institut
    Type: Article , isiRev
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  • 15
    Publication Date: 2022-05-25
    Description: Author Posting. © American Geophysical Union, 2017. This article is posted here by permission of American Geophysical Union for personal use, not for redistribution. The definitive version was published in Journal of Geophysical Research: Oceans 122 (2017): 372–389, doi:10.1002/2016JC012373.
    Description: The Gulf of Maine (GoME) is a shelf region especially vulnerable to ocean acidification (OA) due to natural conditions of low pH and aragonite saturation states (Ω-Ar). This study is the first to assess the major oceanic processes controlling seasonal variability of the carbonate system and its linkages with pteropod abundance in Wilkinson Basin in the GoME. Two years of seasonal sampling cruises suggest that water-column carbonate chemistry in the region undergoes a seasonal cycle, wherein the annual cycle of stratification-overturn, primary production, respiration-remineralization and mixing all play important roles, at distinct spatiotemporal scales. Surface production was tightly coupled with remineralization in the benthic nepheloid layer during high production seasons, which results in occasional aragonite undersaturation. From spring to summer, carbonate chemistry in the surface across Wilkinson Basin reflects a transition from a production-respiration balanced system to a net autotropic system. Mean water-column Ω-Ar and abundance of large thecosomatous pteropods show some correlation, although patchiness and discrete cohort reproductive success likely also influence their abundance. Overall, photosynthesis-respiration is the primary driving force controlling Ω-Ar variability during the spring-to-summer transition as well as over the seasonal cycle. However, calcium carbonate (CaCO3) dissolution appears to occur near bottom in fall and winter when bottom water Ω-Ar is generally low but slightly above 1. This is accompanied by a decrease in pteropod abundance that is consistent with previous CaCO3 flux trap measurements. The region might experience persistent subsurface aragonite undersaturation in 30–40 years under continued ocean acidification.
    Description: Coastal Ocean Institute at Woods Hole Oceanographic Institution; National Science Foundation Grant Number: (OCE-1316040)
    Description: 2017-07-22
    Keywords: Ocean acidification ; Carbonate chemistry ; Aragonite saturation ; Pteropod ; Gulf of Maine ; Wilkinson Basin
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 16
    Publication Date: 2022-05-25
    Description: © The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 9 (2012): 747-757, doi:10.5194/bg-9-747-2012.
    Description: Shelled pteropods (Thecosomata) are a group of holoplanktonic mollusks that are believed to be especially sensitive to ocean acidification because their aragonitic shells are highly soluble. Despite this concern, there is very little known about the physiological response of these animals to conditions of elevated carbon dioxide. This study examines the oxygen consumption and ammonia excretion of five pteropod species, collected from tropical regions of the Pacific Ocean, to elevated levels of carbon dioxide (0.10%, 1000 ppm). Our results show that pteropods that naturally migrate into oxygen minimum zones, such as Hyalocylis striata, Clio pyramidata, Cavolinia longirostris and Creseis virgula, were not affected by carbon dioxide at the levels and duration tested. Diacria quadridentata, which does not migrate, responds to high carbon dioxide conditions with reduced oxygen consumption and ammonia excretion. This indicates that the natural chemical environment of individual species may influence their resilience to ocean acidification.
    Description: Funding of the National Science Foundation (grant OCE-0526502 to Wishner and Seibel, OCE – 0526545 to Daly, and OCE – 0851043 to Seibel), the University of Rhode Island, and the Rhode Island Experimental Program to Stimulate Competitive Research Fellowship Program.
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 17
    Publication Date: 2022-05-25
    Description: © The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS ONE 8 (2013): e53889, doi:10.1371/journal.pone.0053889.
    Description: 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.
    Description: This material is based upon work supported by the National Science Foundation under Grant Number OCE-0928801. AEM was funded through the WHOI Postdoctoral Scholarship. Support to LBB was provided by the College of Liberal Arts & Sciences, University of Connecticut; and by the Census of Marine Life/Alfred P. Sloan Foundation.
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 18
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here by permission of Elsevier for personal use, not for redistribution. The definitive version was published in Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 16 (2015): 1-9, doi:10.1016/j.cbd.2015.06.002.
    Description: Thecosome pteropods, a group of calcifying holoplanktonic molluscs, 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 (~380 ppm) and elevated CO2 (~800 ppm, similar to levels experienced during a diel vertical migration) for ~10 hrs. 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 molluscs, 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.
    Description: The Extreme Science and Engineering Discovery Environment (XSEDE), which is supported by National Science Foundation grant number OCI-1053575, provided computing resources for the differential expression analysis. This material is based upon work supported by the National Science Foundation’s Ocean Acidification Program under grant number OCE-1041068 (to Lawson, Wang, Lavery, and Wiebe), the Woods Hole Oceanographic Institution’s Access to the Sea program (to Tarrant, Maas and Lawson) and the WHOI postdoctoral scholarship program (to Maas).
    Keywords: Acidification ; Climate change ; Gastropod ; Lectin ; Mollusc ; RNA-seq ; Transcriptomics
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 19
    Publication Date: 2022-05-25
    Description: Author Posting. © The Author(s), 2017. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in ICES Journal of Marine Science 74 (2017): 1893–1905, doi:10.1093/icesjms/fsx008.
    Description: Shelled pteropods are planktonic molluscs that may be affected by ocean acidification. Limacina retroversa from the Gulf of Maine were used to investigate the impact of elevated carbon dioxide (CO2) on shell condition as well as swimming and sinking behaviours. Limacina retroversa were maintained at either ambient (ca. 400 μatm) or two levels of elevated CO2 (800 and 1200 μatm) for up to four weeks, and then examined for changes in shell transparency, sinking speed, and swimming behaviour assessed through a variety of metrics (e.g., speed, path tortuosity, wing beat frequency). After exposures to elevated CO2 for as little as four days, the pteropod shells were significantly darker and more opaque in the elevated CO2 treatments. Sinking speeds were significantly slower for pteropods exposed to medium and high CO2 in comparison to the ambient treatment. Swimming behaviour showed less clear patterns of response to treatment and duration of exposure, but overall, swimming did not appear to be hindered under elevated CO2. Sinking is used by L. retroversa for predator evasion, and altered speeds and increased visibility could increase the susceptibility of pteropods to predation.
    Description: Funding for this research was provided by a National Science Foundation grant to Lawson, Maas, and Tarrant (OCE-1316040). Additional support for field sampling was provided by the WHOI Coastal Ocean Institute, Pickman Foundation, and the Tom Haas Fund at the New Hampshire Charitable Foundation.
    Keywords: Ocean acidification ; Shell condition ; Locomotion ; Thecosome pteropod
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 20
    Publication Date: 2022-05-25
    Description: Author Posting. © University of Chicago, 2018. This article is posted here by permission of University of Chicago for personal use, not for redistribution. The definitive version was published in Biological Bulletin 235 (2018): 30-42, doi:10.1086/699219.
    Description: The diel vertical migration of zooplankton is a process during which individuals spend the night in surface waters and retreat to depth during the daytime, with substantial implications for carbon transport and the ecology of midwater ecosystems. The physiological consequences of this daily pattern have, however, been poorly studied beyond investigations of speed and the energetic cost of swimming. Many other processes are likely influenced, such as fuel use, energetic trade-offs, underlying diel (circadian) rhythms, and antioxidant responses. Using a new reference transcriptome, proteomic analyses were applied to compare the physiological state of a migratory copepod, Pleuromamma xiphias, immediately after arriving to the surface at night and six hours later. Oxygen consumption was monitored semi-continuously to explore underlying cyclical patterns in metabolic rate under dark-dark conditions. The proteomic analysis suggests a distinct shift in physiology that reflects migratory exertion and changes in metabolism. These proteomic analyses are supported by the respiration experiments, which show an underlying cycle in metabolic rate, with a peak at dawn. This project generates molecular tools (transcriptome and proteome) that will allow for more detailed understanding of the underlying physiological processes that influence and are influenced by diel vertical migration. Further, these studies suggest that P. xiphias is a tractable model for continuing investigations of circadian and diel vertical migration influences on plankton physiology. Previous studies did not account for this cyclic pattern of respiration and may therefore have unrepresented respiratory carbon fluxes from copepods by about 24%.
    Description: Funding for ET-S was provided by a Training Grant from the National Institutes of Health (T32 HG00035), and proteomics work was supported in part by the University of Washington’s Proteomics Resource (UWPR95794). Funding was provided by Simon’s Foundation International as part of the BIOSSCOPE project.
    Description: 2019-08-16
    Repository Name: Woods Hole Open Access Server
    Type: Article
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