Distribution, patchiness, and behavior of Antarctic zooplankton, assessed using multi-frequency acoustic techniques

Submitted to the MIT Department of Biology and the WHOI Biology Department in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 2006The physical and biological forces that drive zooplankton distribution and patchiness in an antarctic continental shelf region were examined, with particular emphasis on the Antarctic krill, Euphausia superba. This was accomplished by the application of acoustic, video, and environmental sensors during surveys of the region in and around Marguerite Bay, west of the Antarctic Peninsula, in the falls and winters of 2001 and 2002. An important component of the research involved the development and verification of methods for extracting estimates of ecologically-meaningful quantities from measurements of scattered sound. The distribution of acoustic volume backscattering at the single frequency of 120 kHz was first examined as an index of the overall biomass of zooplankton. Distinct spatial and seasonal patterns were observed that coincided with advective features. Improved parameterization was then achieved for a theoretical model of Antarctic krill target strength, the quantity necessary in scaling measurements of scattered sound to estimates of abundance, through direct measurement of all necessary model parameters for krill sampled in the study region and survey period. Methods were developed for identifying and delineating krill aggregations, allowing the distribution of krill to be distinguished from that of the overall zooplankton community. Additional methods were developed and verified for estimating the length, abundance, and biomass of krill in each acoustically-identified aggregation. These methods were applied to multifrequency acoustic survey data, demonstrating strong seasonal, inter-annual, and spatial variability in the distribution of krill biomass. Highest biomass was consistently associated with regions close to land where temperatures at depth were cool. Finally, the morphology, internal structure, and vertical position of individual krill aggregations were examined. The observed patterns of variability in aggregation characteristics between day and night, regions of high versus low food availability, and in the presence or absence of predators, together reinforced the conclusion that aggregation and diel vertical migration represent strategies to avoid visual predators, while also allowing the krill access to shallowly-distributed food resources. The various findings of this work have important implications to the fields of zooplankton acoustics and Antarctic krill ecology, especially in relation to the interactions of the krill with its predators.Funding was provided by a Fulbright Scholarship, a Natural Sciences and Engineering Research Council of Canada Post-Graduate Scholarship, an Office of Naval Research Graduate Traineeship Award in Ocean Acoustics (Grant N00014-03-1-0212), the Comer Science and Education Foundation, and the Woods Hole Oceanographic Institution (WHOI) Academic Programs Office

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

Author Posting. © Acoustical Society of America, 2016. This article is posted here by permission of Acoustical Society of America for personal use, not for redistribution. The definitive version was published in Journal of the Acoustical Society of America 139 (2016): 2885, doi:10.1121/1.4948759.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.This work was supported by the National Science Foundation under Grant No. OCE-0928801 and the NOAA National Marine Fisheries Service, Northwest Fisheries Science Center. G.L.L. was partially supported by NOAA Cooperative Agreement Nos. NA09OAR4320129 and NA14OAR4320158 through the NOAA Fisheries Quantitative Ecology and Socioeconomics Training (QUEST) program

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

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.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.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)

Wideband (15–260 kHz) acoustic volume backscattering spectra of Northern krill (Meganyctiphanes norvegica) and butterfish (Peprilus triacanthus)

This paper is not subject to U.S. copyright. The definitive version was published in ICES Journal of Marine Science 74 (2017): 2249–2261, doi:10.1093/icesjms/fsx050.Measurements of acoustic backscatter made over a wide frequency band have the potential for improved classification relative to traditional narrowband methods, by characterizing more fully the frequency response of scatterers. In January 2014, five wideband transceivers [Simrad EK80 Wideband Transceivers (WBTs)] and split-beam transducers with nominal centre frequencies of 18, 38, 70, 120, and 200 kHz were used to collect acoustic data spanning a nearly continuous 15–260 kHz bandwidth. The acoustic samples were from ca. 2 m below the surface to the seabed in an area along the US continental shelf break. Bottom trawls and zooplankton nets were also used to sample scatterers contributing to selected features of the acoustic backscatter. Measurements of frequency-dependent volume backscattering strength (i.e. volume backscattering spectra) from aggregations of euphausiids (mostly Northern krill, Meganyctiphanes norvegica) clearly resolved the transition from Rayleigh to geometric scattering, consistent with modelled backscatter from the type and length of animals sampled with bongo nets. Volume backscattering spectra from aggregations dominated by butterfish (Peprilus triacanthus) revealed a frequency response that was suggestive of superimposed scattering by soft tissue and bone. Backscatter predicted by Kirchhoff ray mode models of butterfish corresponded to trends in the measured spectra, supporting the assumption that acoustic scattering by butterfish is dominated by soft tissue and vertebrae.NOAA Advanced Sampling Technology Working Group (ASTWG) provided support for this project. GLL was partially supported by NOAA Cooperative Agreements NA09OAR4320129 and NA14OAR4320158 through the NOAA Fisheries Quantitative Ecology and Socioeconomics Training (QUEST) programme

The metabolic response of thecosome pteropods from the North Atlantic and North Pacific oceans to high CO2 and low O2

© The Author(s), 2016. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 13 (2016): 6191-6210, doi:10.5194/bg-13-6191-2016.As anthropogenic activities directly and indirectly increase carbon dioxide (CO2) and decrease oxygen (O2) concentrations in the ocean system, it becomes important to understand how different populations of marine animals will respond. Water that is naturally low in pH, with a high concentration of carbon dioxide (hypercapnia) and a low concentration of oxygen, occurs at shallow depths (200–500 m) in the North Pacific Ocean, whereas similar conditions are absent throughout the upper water column in the North Atlantic. This contrasting hydrography provides a natural experiment to explore whether differences in environment cause populations of cosmopolitan pelagic calcifiers, specifically the aragonitic-shelled pteropods, to have a different physiological response when exposed to hypercapnia and low O2. Using closed-chamber end-point respiration experiments, eight species of pteropods from the two ocean basins were exposed to high CO2 ( ∼  800 µatm) while six species were also exposed to moderately low O2 (48 % saturated, or  ∼  130 µmol kg−1) and a combined treatment of low O2/high CO2. None of the species tested showed a change in metabolic rate in response to high CO2 alone. Of those species tested for an effect of O2, only Limacina retroversa from the Atlantic showed a response to the combined treatment, resulting in a reduction in metabolic rate. Our results suggest that pteropods have mechanisms for coping with short-term CO2 exposure and that there can be interactive effects between stressors on the physiology of these open ocean organisms that correlate with natural exposure to low O2 and high CO2. These are considerations that should be taken into account in projections of organismal sensitivity to future ocean conditions.This work was funded by the National Science Foundation’s Ocean Acidification Program (grant OCE-1041068), the National Institute of Standards and Technology (NIST-60NANB10D024), and the WHOI postdoctoral scholarship program

Evidence of resource partitioning between humpback and minke whales around the western Antarctic Peninsula

Author Posting. © The Author(s), 2009. This is the author's version of the work. It is posted here by permission of John Wiley & Sons for personal use, not for redistribution. The definitive version was published in Marine Mammal Science 25 (2009): 402-415, doi:10.1111/j.1748-7692.2008.00263.x.For closely related sympatric species to coexist, they must differ to some degree in their ecological requirements or niches (e.g., diets) to avoid inter-specific competition. Baleen whales in the Antarctic feed primarily on krill, and the large sympatric pre-whaling community suggests resource partitioning among these species or a non-limiting prey resource. In order to examine ecological differences between sympatric humpback and minke whales around the Western Antarctic Peninsula, we made measurements of the physical environment, observations of whale distribution, and concurrent acoustic measurements of krill aggregations. Mantel’s tests and Classification and regression tree models indicate both similarities and differences in the spatial associations between humpback and minke whales, environmental features, and prey. The data suggest (1) similarities (proximity to shore) and differences (prey abundance versus deep water temperatures) in horizontal spatial distribution patterns, (2) unambiguous vertical resource partitioning with minke whales associating with deeper krill aggregations across a range of spatial scales, and (3) that interference competition between these two species is unlikely. These results add to the paucity of ecological knowledge relating baleen whales and their prey in the Antarctic and should be considered in conservation and management efforts for Southern Ocean cetaceans and ecosystems.This research was supported by the International Whaling Commission, the Duke University Marine Laboratory, NSF US Antarctic Program Grant OPP-9910307 as part of the Southern Ocean GLOBEC project, and a Fulbright Scholarship and Office of Naval Research Grant N00014-03-1-0212 (to G. Lawson)

Exploiting signal processing approaches for broadband echosounders

© International Council for the Exploration of the Sea, 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in ICES Journal of Marine Science 74 (2017): 2262–2275, doi:10.1093/icesjms/fsx155.Broadband echosounders, which transmit frequency-modulated pulses, increase the spectral characterization of targets relative to narrowband echosounders, which typically transmit single-frequency pulses, and also increase the range resolution through broadband matched-filter signal processing approaches. However, the increased range resolution does not necessarily lead to improved detection and characterization of targets close to boundaries due to the presence of undesirable signal processing side lobes. The standard approach to mitigating the impact of processing side lobes is to transmit tapered signals, which has the consequence of also reducing spectral information. To address this, different broadband signal processing approaches are explored using data collected in a large tank with both a Kongsberg–Simrad EK80 scientific echosounder with a combination of single- and split-beam transducers with nominal centre frequencies of 18, 38, 70, 120, 200, and 333 kHz, and with a single-beam custom-built echosounder spanning the frequency band from 130 to 195 kHz. It is shown that improved detection and characterization of targets close to boundaries can be achieved by using modified replica signals in the matched filter processing. An additional benefit to using broadband echosounders involves exploiting the frequency dependence of the beam pattern to calibrate single-beam broadband echosounders using an off-axis calibration sphere.This research was supported by the NOAA Office of Science and Technology, Advanced Sampling Technology Working Group. G.L.L. was partially supported by NOAA Cooperative Agreements NA09OAR4320129 and NA14OAR4320158 through the NOAA Fisheries Quantitative Ecology and Socieconomics Training (QUEST) program. A.C.L. was partially supported through the Office of Naval Research Ocean Acoustics Program

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

Author Posting. © The Company of Biologists, 2018. This article is posted here by permission of The Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 221 (2018): jeb164400, doi:10.1242/jeb.164400.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.Funding for this research was provided by a National Science Foundation grant to G.L.L., A.E.M. and A.M.T. (OCE-1316040). Additional support for field sampling was provided by theWoods Hole Oceanographic Institution, Coastal Ocean Institute and the Pickman Foundation.2019-02-1

The effect of elevated carbon dioxide on the sinking and swimming of the shelled pteropod Limacina retroversa

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.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.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

Life cycle and early development of the thecosomatous pteropod Limacina retroversa in the Gulf of Maine, including the effect of elevated CO2 levels

Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Marine Biology 162 (2015): 2235-2249, doi:10.1007/s00227-015-2754-1.Thecosome pteropods are pelagic molluscs with aragonitic shells. They are considered to be especially vulnerable among plankton to ocean acidification (OA), but to recognize changes due to anthropogenic forcing a baseline understanding of their life history is needed. In the present study, adult Limacina retroversa were collected on five cruises from multiple sites in the Gulf of Maine (between 42° 22.1’–42° 0.0’ N and 69° 42.6’–70° 15.4’ W; water depths of ca. 45–260 m) from October 2013−November 2014. They were maintained in the laboratory under continuous light at 8° C. There was evidence of year-round reproduction and an individual life span in the laboratory of 6 months. Eggs laid in captivity were observed throughout development. Hatching occurred after 3 days, the veliger stage was reached after 6−7 days, and metamorphosis to the juvenile stage was after ~ 1 month. Reproductive individuals were first observed after 3 months. Calcein staining of embryos revealed calcium storage beginning in the late gastrula stage. Staining was observed in the shell gland, shell field, mantle, and shell margin in later stages. Exposure of two batches of larvae at the gastrula stage to elevated CO2 levels (800 and 1200 ppm) resulted in significantly increased mortality in comparison with individuals raised under ambient (~400 ppm) conditions and a developmental delay in the 1200 ppm treatment compared with the ambient and 800 ppm treatments.A. Thabet is grateful for a fellowship from the Egyptian Culture and Education Bureau and for mentoring from Drs. S.A. Saber, M.M. Sarhan and M.M. Fouda. 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 and Pickman Foundation to Wang, Maas, and Lawson.2016-10-2