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  • 1
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    Pieces in a global puzzle: population genetics at two whale shark aggregations in the western Indian Ocean (2022)
    Wiley Open Access
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2022. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Hardenstine, R., He, S., Cochran, J., Braun, C., Cagua, E., Pierce, S., Prebble, C., Rohner, C., Saenz‐Angudelo, P., Sinclair‐Taylor, T., Skomal, G., Thorrold, S., Watts, A., Zakroff, C., & Berumen, M. Pieces in a global puzzle: population genetics at two whale shark aggregations in the western Indian Ocean. Ecology and Evolution, 12(1), (2022): e8492, https://doi.org/10.1002/ece3.8492.
    Description: The whale shark Rhincodon typus is found throughout the world's tropical and warm-temperate ocean basins. Despite their broad physical distribution, research on the species has been concentrated at a few aggregation sites. Comparing DNA sequences from sharks at different sites can provide a demographically neutral understanding of the whale shark's global ecology. Here, we created genetic profiles for 84 whale sharks from the Saudi Arabian Red Sea and 72 individuals from the coast of Tanzania using a combination of microsatellite and mitochondrial sequences. These two sites, separated by approximately 4500 km (shortest over-water distance), exhibit markedly different population demographics and behavioral ecologies. Eleven microsatellite DNA markers revealed that the two aggregation sites have similar levels of allelic richness and appear to be derived from the same source population. We sequenced the mitochondrial control region to produce multiple global haplotype networks (based on different alignment methodologies) that were broadly similar to each other in terms of population structure but suggested different demographic histories. Data from both microsatellite and mitochondrial markers demonstrated the stability of genetic diversity within the Saudi Arabian aggregation site throughout the sampling period. These results contrast previously measured declines in diversity at Ningaloo Reef, Western Australia. Mapping the geographic distribution of whale shark lineages provides insight into the species’ connectivity and can be used to direct management efforts at both local and global scales. Similarly, understanding historical fluctuations in whale shark abundance provides a baseline by which to assess current trends. Continued development of new sequencing methods and the incorporation of genomic data could lead to considerable advances in the scientific understanding of whale shark population ecology and corresponding improvements to conservation policy.
    Description: Work in Saudi Arabia was funded in part by KAUST baseline research funds (to MLB), KAUST award nos. USA00002 and KSA 00011 (to SRT), and the U.S. National Science Foundation (OCE 0825148 to SRT and GBS).
    Keywords: genetic diversity ; global population structure ; microsatellites ; mtDNA ; Rhincodon typus
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 2
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    Physiological and behavioral responses, and their variability, in squid, Doryteuthis pealeii, embryos and paralarvae reared under chronic ocean acidification (2019)
    Massachusetts Institute of Technology and Woods Hole Oceanographic Institution
    Details
    Publication Date: 2022-05-26
    Description: Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Oceanography at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 2019.
    Description: Ocean acidification (OA) and related stressors, like warming, are occurring rapidly in coastal systems. There is concern about the impacts these stressors may have on the early development of species that use the nearshore as nursery habitat. The inshore longfin squid, Doryteuthis pealeii, plays an important role in the northwest Atlantic food web, and annually lays its eggs in the nearshore benthos during summer. This thesis sought to characterize morphological, physiological, and behavioral responses of D. pealeii embryos and paralarvae to OA. Experiments began in 2013, where I exposed squid eggs to a range of acidification levels (400 - 2200 ppm CO2) to uncover when the dosage impacts first appear (around 1300 ppm). To do this, I developed multiple methods to better characterize the morphological changes and surface degradation of statoliths due to acidification. This initial work demonstrated small-scale variability in response intensity, across hatching days and the breeding season. I ran swimming behavior experiments with subsampled paralarvae from 2013 - 2015 and developed a novel 3D recording and analysis tracking system in the process. The 2D data from 2013 showed significant decreases in time spent near surface, while 3D data in subsequent years showed slight impacts to activity and swimming velocity with increasing acidification. Overall, I ran experiments from 2013-2016, and compiled and compared these data using response ratios. I show that seasonal temperatures impact the baseline state of the paralarvae through parental condition, while acidification sensitivity appears driven by parental year class. Finally, I examined the interaction of acidification stress with warming, demonstrating an antagonistic relationship between these stressors for this life stage of this squid. These data indicate that acidification builds as a stressor, impacting late stages of embryonic development, while warming impacts embryos early in development, and likely reduces acidification impacts by decreasing development time. This dissertation demonstrates that while the embryonic and paralarval stages can be sensitive to acidification, being so highly fecund and varying in resistance at multiple temporal scales allows for a substantial potential for resilience to a changing ocean in this population of squid.
    Description: The National Science Foundation provided funding for this project under Grant No. 1220034 to Aran Mooney. The Woods Hole Oceanographic Institution also funded research presented in this dissertation through the Coastal Ocean Institute and Grassle Family Foundation awards. The National Science Foundation Graduate Research Fellowship provided tuition and stipend support under Grant No. 1122374. The Hugh Hampton Young Memorial Fund Fellowship provided through the MIT Office of Graduate Education also provided tuition and stipend support, as did the Academic Programs Office of the Woods Hole Oceanographic Institution. The Mindlin Foundation, through their OneTweetOnePercent award, and the Academic Programs Office of the Woods Hole Oceanographic Institution provided support for time pursuing outreach and science communication projects.
    Keywords: Ocean acidification ; Ocean temperature ; Habitat (Ecology) ; Squids
    Repository Name: Woods Hole Open Access Server
    Type: Thesis
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  • 3
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    Ocean acidification responses in paralarval squid swimming behavior using a novel 3D tracking system (2019)
    Springer Nature
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © The Author(s), 2019. This is the author's version of the work. It is posted here by permission of Springer Nature for personal use, not for redistribution. The definitive version was published in Zakroff, C., Mooney, T.A. & Wirth, C. Ocean acidification responses in paralarval squid swimming behavior using a novel 3D tracking system. Hydrobiologia, 808(1),(2018):83-106, doi:10.1007/s10750-017-3342-9.
    Description: Chronic embryonic exposure to ocean acidification (OA) has been shown to degrade the aragonitic statolith of paralarval squid, Doryteuthis pealeii, a key structure for their swimming behavior. This study examined if day-of-hatching paralarval D. pealeii from eggs reared under chronic OA demonstrated measurable impairments to swimming activity and control. This required the development of a novel, cost-effective, and robust method for 3D motion tracking and analysis. Squid eggs were reared in pCO2 levels in a dose-dependent manner ranging from 400 - 2200 ppm. Initial 2D experiments showed paralarvae in higher acidification environments spent more time at depth. In 3D experiments, velocity, particularly positive and negative vertical velocities, significantly decreased from 400 to 1000 ppm pCO2, but showed non-significant decreases at higher concentrations. Activity and horizontal velocity decreased linearly with increasing pCO2, indicating a subtle impact to paralarval energetics. Patterns may have been obscured by notable individual variability in the paralarvae. Responses were also seen to vary between trials on cohort or potentially annual scales. Overall, paralarval swimming appeared resilient to OA, with effects being slight. The newly developed 3D tracking system provides a powerful and accessible method for future studies to explore similar questions in the larvae of aquatic taxa.
    Description: We thank D. Remsen, the MBL Marine Resources Center staff, and MBL Gemma crew for their support in acquiring squid. R. Galat and the facilities staff of the WHOI ESL provided system support. D. McCorkle, KYK Chan, and M. White provided valuable insight on the OA system. E. Moberg, A. Beet, and A. Solow assisted in the development and coding of the 3D model system. We also thank E. Bonk, K. Hoering, M. Lee, D. Weiler, and A. Schlunk for their assistance and input with the experiments. This material is based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. 1122374. This project is funded by NSF Grant No. 1220034.
    Keywords: Hypercapnia ; Cephalopod ; Larvae ; Movement analysis ; Stress physiology
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 4
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    Dose-dependence and small-scale variability in responses to ocean acidification during squid, Doryteuthis pealeii, development (2019)
    Springer
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © The Author(s), 2019. 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 , Zakroff, C., Mooney, T.A. & Berumen, M.L. Dose-dependence and small-scale variability in responses to ocean acidification during squid, Doryteuthis pealeii, development. Marine Biology, (2019), 166: 62. doi:10.1007/s00227-019-3510-8.
    Description: Coastal squids lay their eggs on the benthos, leaving them to develop in a dynamic system that is undergoing rapid acidification due to human influence. Prior studies have broadly investigated the impacts of ocean acidification on embryonic squid, but have not addressed the thresholds at which these responses occur or their potential variability. We raised squid, Doryteuthis pealeii (captured in Vineyard Sound, Massachusetts, USA: 41° 23.370N 70° 46.418´W), eggs in three trials across the breeding season (May - September, 2013) in a total of six chronic pCO2 exposures (400, 550, 850, 1300, 1900, and 2200 ppm). Hatchlings were counted and subsampled for mantle length, yolk volume, hatching time, hatching success, and statolith morphology. New methods for analysis of statolith shape, rugosity, and surface degradation were developed and are presented (with code). Responses to acidification (e.g., reduced mantle lengths, delayed hatching, and smaller, more degraded statoliths) were evident at ~ 1300 ppm CO2. However, patterns of physiological response and energy management, based on comparisons of yolk consumption and growth, varied among trials. Interactions between pCO2 and hatching day indicated a potential influence of exposure time on responses, while interactions with culture vessel highlighted the substantive natural variability within a clutch of eggs. While this study is consistent with, and expands upon, previous findings of sensitivity of the early life stages to acidification, it also highlights the plasticity and potential for resilience in this population of squid.
    Description: This material was based upon work supported by the National Science Foundation Graduate Research Fellowship under Grant No. 1122374 to CZ. This project was funded by National Science Foundation Grant No. 1220034 to TAM.
    Description: 2020-04-19
    Keywords: cephalopod ; embryo ; hypercapnia ; paralarvae ; statolith ; stress
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 5
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    Extreme low oxygen and decreased pH conditions naturally occur within developing squid egg capsules (2016)
    Details
    Publication Date: 2022-05-26
    Description: Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here by permission of Inter-Research for personal use, not for redistribution. The definitive version was published in Marine Ecology Progress Series 550 (2016): 111-119, doi:10.3354/meps11737.
    Description: Young animals found future cohorts and populations but are often particularly susceptible to environmental changes. This raises concerns that future conditions, influenced by anthropogenic changes such as ocean acidification and increasing oxygen minimum zones, will greatly affect ecosystems by impacting developing larvae. Understanding the potential impacts requires addressing present tolerances and the current conditions in which animals develop. Here, we examined the changes in oxygen and pH adjacent to and within normally-developing squid egg capsules, providing the first observations that the egg capsules, housing hundreds of embryos, had extremely low internal pH (7.34) and oxygen concentrations (1.9 μmol L-1). While early-stage egg capsules had pH and oxygen levels significantly lower than the surrounding seawater, late-stage capsules dropped dramatically to levels considered metabolically stressful even for adults. The structure of squid egg capsules resulted in a closely packed unit of respiring embryos, which likely contributed to the oxygen-poor and CO2-rich local environment. These conditions rivaled the extremes found in the squids’ natural environment, suggesting they may already be near their metabolic limit and that these conditions may induce a hatching cue. While squid may be adapted to these conditions, further climate change could place young, keystone squid outside of their physiological limits.
    Description: This work was supported by a NSF Ocean Acidification grant (#1220034; TAM) and the WHOI Ocean Climate Change Institute (Ocean Acidification Initiative; MHL).
    Description: 2017-05-25
    Keywords: Cephalopod ; Climate change ; Hypoxia ; Boundary layer ; Eggs ; Larva
    Repository Name: Woods Hole Open Access Server
    Type: Preprint
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  • 6
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    Antagonistic interactions and clutch-dependent sensitivity induce variable responses to ocean acidification and warming in squid (Doryteuthis pealeii) embryos and paralarvae (2020)
    Frontiers Media
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Zakroff, C. J., & Mooney, T. A. Antagonistic interactions and clutch-dependent sensitivity induce variable responses to ocean acidification and warming in squid (Doryteuthis pealeii) embryos and paralarvae. Frontiers in Physiology, 11, (2020): 501, doi:10.3389/fphys.2020.00501.
    Description: Ocean acidification (OA) and warming seas are significant concerns for coastal systems and species. The Atlantic longfin squid, Doryteuthis pealeii, a core component of the Northwest Atlantic trophic web, has demonstrated impacts, such as reduced growth and delayed development, under high chronic exposure to acidification (2200 ppm), but the combined effects of OA and warming have not been explored in this species. In this study, D. pealeii egg capsules were reared under a combination of several acidification levels (400, 2200, and 3500 ppm) and temperatures (20 and 27°C). Hatchlings were measured for a range of metrics [dorsal mantle length (DML), yolk sac volume (YV), malformation, and hatching success] in three trials over the 2016 breeding season (May – October). Although notable resistance to stressors was seen, highlighting variability within and between clutches, reduced DML and malformation of the embryos occurred at the highest OA exposure. Surprisingly, increased temperatures did not appear to exacerbate OA impacts, although responses were variable. Time to hatching, which increased with acidification, decreased much more drastically under warming and, further, decreased or removed delays caused by acidification. Hatching success, while variable by clutch, showed consistent patterns of greater late stage loss of embryos under acidification and greater early stage loss under warming, highlighting the potential difference in timing between these stressors for this system, i.e., that acidification stress builds up and causes impacts over time within the egg capsule as the embryos grow and respire. High OA-exposed hatchlings from the warmer conditions often showed reduced impacts compared to those reared in ambient temperatures. This may be due to the increased developmental rate and subsequently reduced OA exposure time of embryos in the higher temperature treatment. These results indicate a substantive potential plasticity to multiple stressors during the embryonic development of this species of squid, but do not predict how this species would fare under these future ocean scenarios.
    Description: This research was supported by the National Science Foundation Grant No. 1220034 to TM and the National Science Foundation Graduate Research Fellowship under Grant No. 1122374 to CZ.
    Keywords: cephalopod ; hypercapnia ; Myopsida ; temperature ; stress ; multifactor ; malformation
    Repository Name: Woods Hole Open Access Server
    Type: Article
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