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Pteropod Shell Condition, Locomotion, and Long-Term Population Trends

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Pteropod Shell Condition, Locomotion, and Long-Term Population Trends Pteropod Shell Condition, Locomotion, and Long-term Population Trends in the Context of Ocean Acidification and Environmental Change By Alexander Bergan B.S., University of California San Diego, 2010 Submitted 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 June 2017 © 2017 Alexander J. Bergan All rights reserved. The author hereby grants to MIT and WHOI permission to reproduce and to distribute publicly paper and electronic copies of this thesis document in whole or in part in any medium now known or hereafter created. Signature of Author ______________________________________________________________________________ Joint Program in Biological Oceanography Massachusetts Institute of Technology and Woods Hole Oceanographic Institution May 24, 2017 Certified by ______________________________________________________________________________ Gareth L. Lawson Thesis Supervisor, Joint Committee for Biology Department Woods Hole Oceanographic Institution Accepted by ______________________________________________________________________________ Ann M. Tarrant Chair, Joint Committee for Biology Department Woods Hole Oceanographic Institution 2 Pteropod Shell Condition, Locomotion, and Long-term Population Trends in the Context of Ocean Acidification and Environmental Change By Alexander Bergan Submitted to the MIT-WHOI Joint Program in Oceanography and Applied Ocean Science and Engineering, in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biological Oceanography Abstract Thecosome pteropods are planktonic mollusks that form aragonite shells and that may experience increased dissolution and other adverse effects due to ocean acidification. This thesis focuses on assessing the possible biological effects of ocean acidification on the shells and locomotion of pteropods and examining the response of a local pteropod population to environmental change over time. I analyzed shell condition after exposing pteropods to elevated CO2 as well as in natural populations to investigate the sensitivity of the shells of different species to aragonite saturation state (ΩA). The pteropods (Limacina retroversa) from laboratory experiments showed the clearest pattern of shell dissolution in response to decreased ΩA, while wild populations either had non-significant regional trends in shell condition (Clio pyramidata) or variability in shell condition that did not match expectations due to regional variability in ΩA (Limacina helicina). At locations with intermediate ΩA (1.5-2.5) the variability seen in L. helicina shell condition might be affected by food availability more than ΩA. I examined sinking and swimming behaviors in the laboratory in order to investigate a possible fitness effect of ocean acidification on pteropods. The sinking rates of L. retroversa from elevated CO2 treatments were slower in conjunction with worsened shell condition. These changes could increase their vulnerability to predators in the wild. Swimming ability was mostly unchanged by elevated CO2 after experiments that were up to three weeks in duration. I used a long-term dataset of pteropods in the Gulf of Maine to directly test whether there has been a population effect of environmental change over the past several decades. I did not observe a population decline between 1977 and 2015, and L. retroversa abundance in the fall actually increased over the time series. Analysis of the habitat use of L. retroversa revealed seasonal associations with temperature, salinity, and bottom depths. The combination of laboratory experiments and field surveys helped to address gaps in knowledge about pteropod ecology and improve our understanding of the effects of ocean acidification on pteropods. Thesis supervisor: Gareth L. Lawson Title: Associate Scientist, Woods Hole Oceanographic Institution 3 4 Acknowledgements I would like to thank my adviser, G. Lawson, who provided me with all of the opportunities that made this research possible. Also, I would like to thank the other members of my thesis committee, C. Asjian, G. Flierl, and L. Mullineaux, for their guidance and support and M. Neubert for chairing the defense. I would like to acknowledge the help of J. Kellner who served on the thesis committee for most of my candidacy. I would like to thank Captain K. Houtler and Mate I. Hanley of the R/V Tioga, Captain D. Mello and crew of OC473, and Captain I. Lawrence and the crew of NH1208 for all of their efforts that allowed us to collect data and pteropods. I appreciate the help I received at sea and in the lab collecting and rearing the pteropods from P. Alatalo, L. Blanco Bercial, T. Bolmer, S. Chu, N. Copley, T. Crockford, S. Crosby, J. Edebeli, M. Edenius, J. Fincke, K. Hoering, G. Lawson, R. Levine, M. Lowe, C. Luttazi, A. Maas, K. Manganini, C. Pagniello, E. Roberts, L. Roger, A. Schlunk, A. Tarrant, A. Thabet, N. Tuttle, M. Uddin, B. Voss, Z. Wang, T. White, P. Wiebe, K. Wurtzell. I thank R. Galat and D. McCorkle for their help setting up the CO2 exposure system and S. Chu, K. Hoering, K. Morkeski, and Z. Sandwich for their invaluable help measuring carbonate chemistry. I would like to thank K. Young and D. Adhikari for providing insight into how to measure pteropod movements. I also thank S. Colin, J. Costello, H. Jiang, and L. Mullineaux for loaning equipment used for filming. I would like to thank A. Solow for his invaluable help with statistics used for comparing shell condition and habitat usage. I thank L. Kerr, A. Kuzirian, S. Senft, and the technicians at the Central Microscopy Facility at MBL for teaching me how to use their SEM. I would also like to thank V. Le Roux and A. Helbling for teaching me how to use the micro-CT. I would like to acknowledge C. Charette, V. Caron, L. Fraser, K. Kipp, R. Schwartz, M. Tivey, J. Westwater, and J. Yoder for all of their help in the Academic Programs Office. Finally, I would like to thank my family and friends for all of their support along the way. Funding Sources Funding for this research was provided by a National Science Foundation grant to Lawson, Lavery, Wang, and Wiebe (OCE-1041068), a National Science Foundation grant to Lawson, Maas, and Tarrant (OCE-1316040), a WHOI Coastal Ocean Institute Student Research Proposal Award to Bergan (COI-27040178), the Pickman Foundation, the Tom Haas Fund at the New Hampshire Charitable Foundation, and the WHOI Academic Programs Office. 5 6 Table of Contents Abstract ....................................................................................................................................... 3 Acknowledgments ....................................................................................................................... 5 Table of Contents ........................................................................................................................ 7 List of Figures ............................................................................................................................. 9 List of Tables .............................................................................................................................. 10 1. Introduction ..................................................................................................................... 11 1.1 Pteropod Biology ................................................................................................ 11 1.2 Ocean Acidification ............................................................................................ 15 1.3 Calcification and Dissolution .............................................................................. 17 1.4 Pteropod Time Series ........................................................................................... 20 1.5 Study Regions ..................................................................................................... 21 1.6 Objectives ........................................................................................................... 22 2. The effect of elevated carbon dioxide on the sinking and swimming of the shelled pteropod Limacina retroversa ......................................................................................... 29 2.1 Abstract ............................................................................................................... 29 2.2 Introduction ......................................................................................................... 30 2.3 Methods ............................................................................................................... 32 2.4 Results ................................................................................................................. 41 2.5 Discussion ........................................................................................................... 52 2.6 Supplementary Materials .................................................................................... 60 3. Shell condition of three thecosome pteropod species (Limacina retroversa, Limacina helicina, and Clio pyramidata) from CO2 exposure experiments and wild populations 65 3.1 Abstract ............................................................................................................... 65 3.2 Introduction ......................................................................................................... 66 3.3 Methods ..............................................................................................................
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