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UNIVERSITY of CALIFORNIA Los Angeles Design and Implementation of Environmental DNA Metabarcoding Methods for Monitoring the So UNIVERSITY OF CALIFORNIA Los Angeles Design and Implementation of Environmental DNA Metabarcoding Methods for Monitoring the Southern California Marine Protected Area Network A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Philosophy in Biology by Zachary Jacob Gold 2020 © Copyright by Zachary Jacob Gold 2020 ABSTRACT OF THE DISSERTATION Design and Implementation of Environmental DNA Metabarcoding Methods for Monitoring the Southern California Marine Protected Area Network by Zachary Jacob Gold Doctor of Philosophy in Biology University of California, Los Angeles, 2020 Professor Paul Barber, Chair Marine protected areas (MPAs) are important tools for maintaining biodiversity and abundance of marine species. However, key to the effectiveness of MPAs is monitoring of marine communities. Current monitoring methods rely heavily on SCUBA-based visual observations that are costly and time consuming, limiting the scope of MPA monitoring. Environmental DNA (eDNA) metabarcoding is a promising cost effective, rapid, and automatable alternative for marine ecosystem monitoring. However, as a developing tool, the utility of eDNA metabarcoding requires improved bioinformatic techniques and reference barcode databases. Furthermore, it is important to understand how eDNA metabarcoding performs relative to visual surveys to better understand the strengths and limitations of each approach. This thesis improves eDNA metabarcoding approaches to survey the nearshore rocky reef and kelp forest ecosystems within the Southern California MPA network. It then tests the effectiveness of eDNA metabarcoding against visual surveys conducted by the Channel Islands National Park Service ii Kelp Forest Monitoring Program and Reef Check California. In Chapter 1, I develop FishCARD, a 12S reference barcode database specific to fishes of the California Current ecosystem. FishCARD improves eDNA metabarcoding taxonomic assignments, resulting in the identification of a broader array of marine vertebrate diversity, including invasive, endangered, and mobile species frequently missed by visual surveys. In Chapter 2, I compare eDNA metabarcoding and visual underwater survey methods inside, on the edge of, and outside the Scorpion State Marine Reserve off Santa Cruz Island. We demonstrate that eDNA captures a broader range of fish taxa than visual surveys and detects fine-scale spatial differences in fish communities. In Chapter 3, I demonstrate that eDNA metabarcoding and visual underwater surveys capture similar biogeographic patterns of fish communities across 44 sites within the Southern California Bight. Importantly, eDNA methods distinguished fish communities inside and outside of Southern California MPAs, finding a greater abundance of target species inside MPAs matching patterns observed through visual surveys. These results built off the collaborative development of the Anacapa Toolkit metabarcoding pipeline. Together I demonstrate the utility of eDNA metabarcoding for monitoring MPAs, providing an important complementary tool to visual methods, helping expand MPA monitoring across space, time, and depth. iii The dissertation of Zachary Jacob Gold is approved. Peggy Fong Richard F. Ambrose Thomas B. Smith Paul H. Barber, Committee Chair University of California, Los Angeles, 2020 iv In memory of our heroes taken from us far too soon who did their part to make the world a brighter place while protecting and loving our oceans Jonathan Gold, David Klein, Marybeth Guiney, Charles McIlvan, & the 32 other divers onboard the MV Conception v TABLE OF CONTENTS Abstract ................................................................................................................................ ii List of Acronyms ............................................................................................................... vii Glossary ............................................................................................................................ viii List of Tables ...................................................................................................................... ix List of Figures .................................................................................................................... xii Supplementary Materials ................................................................................................. xvii Acknowledgements ........................................................................................................ xviii Biographical Sketch ..................................................................................................... xxxvii Introduction ......................................................................................................................... 1 Chapter 1 ........................................................................................................................... 14 Chapter 2 ........................................................................................................................... 34 Chapter 3 ........................................................................................................................... 61 Conclusion ....................................................................................................................... 115 Supplemental Chapter 1 .................................................................................................. 118 Supplemental Chapter 2 .................................................................................................. 129 Appendix A – Chapter 1 .................................................................................................. 140 Appendix B – Chapter 2 .................................................................................................. 143 Appendix C – Chapter 3 .................................................................................................. 149 Appendix D – Supplemental Chapter 2 ........................................................................... 167 References ....................................................................................................................... 179 vi LIST OF ACRONYMS Acronym Description 12S Small subunit gene of the mitochondrial ribosome 16S Small subunit gene of the mitochondrial ribosome ANOVA Analysis of Variance ASV Amplicon Sequence Variant betadisper Multivariate analogue of Levene’s test for homogeneity of variances BLAST Basic Local Alignment Search Tool CalCOFI California Cooperative Oceanic Fisheries Investigation CAP Analysis Constrained Analysis of Principle components Analysis CO1 Cytochrome C Oxidase subunit 1 gene of mitochondrial DNA CRUX Creating Reference libraries Using eXisting tools software CytB Cytochrome B gene of mitochondrial DNA DNA Deoxyribonucleic acid eDNA environmental DNA FishCARD California fish specific 12S California Reference Barcode Database GPS Global Positioning System MPA Marine Protected Area NCBI National Center for Biotechnology Information NMDS Non-metric Multidimensional Scaling PCR Polymerase Chain Reaction PERMANOVA Permutational Analysis of Variance PISCO Partnership for Interdisciplinary Studies of Coastal Oceans RNA Ribonucleic acid RV Research Vessel SCUBA Self-Contained Underwater Breathing Apparatus SIO Scripps Institution of Oceanography UCLA University of California, Los Angeles vii GLOSSARY Term Description Amplicon short DNA fragment generated from metabarcoding unique DNA sequence recovered from high-throughput Amplicon Sequence Variant metabarcoding inferred as having a true biological origin Barcode Region specific gene locus within the genome a test performed on biologically distinct samples representing Biological Replicate an independent sampling event, i.e. three 1 L water samples collected from the same kelp forest habitat a bioinformatic process to remove non-target sequences Decontamination inadvertently recovered in the processing of field or laboratory samples DNA Barcode short DNA fragment used for species identification a technique based on isolation and sequencing of freely eDNA associated DNA from soil or water samples species classification based on the deepest shared taxonomic Lowest Common Ancestor identification between the best aligned DNA reference Taxonomic Assignment barcodes a process in which multiple species are identified from bulk DNA (e.g., homogeniZed gut contents or settlement tile Metabarcoding scrapings) or environmental DNA (eDNA) samples (e.g., water and soil) typically by PCR amplification and sequencing of a target gene a collection of reference barcode sequences used to assign Reference Barcode Database taxonomy to metabarcoding derived DNA sequences DNA identification sequence obtained from reference Reference Barcode Sequence voucher specimen of known origin and identity a probabilistic model used to determine the true presence or Site Occupancy Model absence of a species at a site given accounting for imperfect survey detection a test performed on the same sample multiple times, i.e. three Technical Replicate PCR reactions using the same extracted DNA sample viii LIST OF TABLES TABLES Chapter 3. Table 3-1. Average Sensitivity and Specificity for eDNA and Visual Survey Methods. Supplemental Chapter 2. Table S2-1. Site Occupancy Modeling Estimated Sensitivity and Specificity of eDNA Metabarcoding and Dip-net Surveys. SUPPLEMENTAL TABLES Chapter 1 Supplemental Tables. Supplemental Table 1-S1. List of California Fish Species.
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