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Dispersal, Fishing, and the Conservation of Marine Species a Dissertation Submitted to the Department of Biology and the Commit DISPERSAL, FISHING, AND THE CONSERVATION OF MARINE SPECIES A DISSERTATION SUBMITTED TO THE DEPARTMENT OF BIOLOGY AND THE COMMITTEE ON GRADUATE STUDIES OF STANFORD UNIVERSITY IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY Malin La Farge Pinsky June 2011 © 2011 by Malin La Farge Pinsky. All Rights Reserved. Re-distributed by Stanford University under license with the author. This work is licensed under a Creative Commons Attribution- Noncommercial 3.0 United States License. http://creativecommons.org/licenses/by-nc/3.0/us/ This dissertation is online at: http://purl.stanford.edu/fk096nf3828 ii I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Stephen Palumbi, Primary Adviser I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Rodolfo Dirzo I certify that I have read this dissertation and that, in my opinion, it is fully adequate in scope and quality as a dissertation for the degree of Doctor of Philosophy. Elizabeth Hadly Approved for the Stanford University Committee on Graduate Studies. Patricia J. Gumport, Vice Provost Graduate Education This signature page was generated electronically upon submission of this dissertation in electronic format. An original signed hard copy of the signature page is on file in University Archives. iii iv Abstract A central goal of ecology is to understand the forces driving the distribution and abundance of organisms. However, understanding the population dynamics of high-dispersal species, their conservation, and the connections between population dynamics and evolution remains difficult. It is in this context that marine organisms provide a particularly intriguing and challenging study system. Their population dynamics are often highly stochastic, most species have a great ability to disperse, and as the last group of wild species exploited commercially, their ecology and evolution can be strongly influenced by human behavior. By using population genetics, modeling, and meta-analysis, this thesis investigates the spatial ecology of reef fish and the causes and evolutionary consequences of global fisheries collapse. One of the first challenges in understanding spatial population dynamics is obtaining accurate measurements of dispersal abilities. This has been especially difficult for marine species with pelagic larvae. In Chapter 1, I apply a new approach to measuring single-generation dispersal kernels in Clark’s anemonefish (Amphiprion clarkii) in the central Philippines (Pinsky et al. 2010 Evolution 64(9): 2688-2700). After developing two methods for measuring the strength of local genetic drift, my results suggest that larval dispersal kernels in A. clarkii had a spread near 11 km (4-27 km). This study shows that ecologically relevant larval dispersal can be estimated with widely available genetic methods when effective density is measured carefully through cohort sampling and ecological censuses. In Chapter 2, I use dispersal kernels to develop a model for population openness. Openness refers to the degree to which populations are replenished by immigrants or by local production, a factor that has strong implications for population dynamics, species interactions, and response to exploitation. It is also a population trait that has been increasingly measured empirically, though we have until now lacked theory for predicting population openness. I show that considering habitat isolation elegantly explains the existence of surprisingly closed populations in high v dispersal species, and that relatively closed populations are expected when patch spacing is more than twice the standard deviation of a species’ dispersal kernel. In addition, empirical scales of habitat patchiness on coral reefs are sufficient to create both largely open and largely closed populations. We predict that habitat patchiness has strong control over population replenishment pathways for a wide range of marine and terrestrial species with a highly dispersive life stage. While the first tow chapters have strong implications for the design of regional marine protected areas, I turn to global conservation questions in Chapters 3 and 4. I first ask which marine fishes are most vulnerable to human impacts (Pinsky et al. 2011 Proceedings of the National Academy of Sciences doi/10.1073/pnas.1015313108). Surveys of terrestrial species have suggested that large-bodied species and top predators are the most at risk, but there has been no global test of this hypothesis in the sea. Contrary to expectations, two datasets compiled from around the world suggest that up to twice as many fisheries for small, low trophic level species have collapsed as compared to those for large predators. I then show that collapsed and overfished species have lower genetic diversity than their close relatives (Pinsky & Palumbi, in prep). While the ecological and ecosystem impacts of harvesting wild populations have long been recognized, it has been controversial how widespread evolutionary impacts are. Using a meta-analytical approach across 37 taxonomically paired comparisons, I find on average 19% fewer alleles per locus in overfished species, but little difference in heterozygosity. I confirm with simulations that these results are consistent with a recent population bottleneck. These results suggest that the genetic impacts of overharvest are widespread, even among abundant species. A loss of allelic richness has implications for the long-term evolutionary potential of species. vi Acknowledgements I could not have completed these last five years without the support, encouragement, and enthusiasm of those around me. While this list is incomplete, I am indebted to: My Advisor Steve Palumbi My Committee Elizabeth Hadly Fiorenza Micheli Steve Gaines Rodolfo Dirzo Chris Lowe Collaborators Olaf Jensen, Dan Ricard, Boris Worm, Ray Hilborn, Trevor Branch, Katie Arkema, Greg Guannel, Mary Ruckelshaus, Anne Guerry, Marcel van Tuinen, Doug Kennett, Seth Newsome, Serge Andréfouët, Humberto Montes, Jr. and the Visayas State University Marine Lab, Amado Blanco and the Project Seahorse Foundation, Rose- Liza Eisma-Osorio and the Coastal Conservation and Education Foundation Colleagues in the Palumbi Lab Melissa Pespeni, Jason Ladner, Carolyn Tepolt, Alison Haupt, Ryan Kelly, Dan Barshis, Tom Oliver, Mollie Manier, Heather Galindo, Liz Alter, Emily Jacobs- Palmer, Kelly Barr, Kristen Ruegg, Vanessa Michelou, Arjun Sivasundar, Pierre De Wit, Marina Oster, Hannah Jaris, Veronica Searles, and Mark Walker My Cohort Julie Stewart, Nishad Jayasundara, Kevin Miklasz, Aaron Carlisle, Posy Busby, Camila Donati, Beth Pringle, and Jason Ladner Hopkins Marine Station Scientists and Staff Kristy Kroeker, Cheryl Logan, Judit Pungor, Giulio de Leo, Salvador Jorgensen, Chelsea Wood, Steve Litvin, Doug McCauley, Mark Denny, Ashley Greenley, Ashley vii Booth, Tom Hata, Megan Jensen, Ishbel Kerkez, Dane Klinger, Judy Thompson, Joe Wible, Doreen Zelles, Chris Patton, Freya Sommer, Carol Reeb, John Lee, Jim Watanabe, Bob Doudna, Peter Ferrante, Barbara Compton, and Vicki Pearse Stanford University Scientists and Staff Jessica Blois, Judsen Bruzgul, Sarah McMenamin, Paula Spaeth, Lily Li, Dmitri Petrov, Valeria Kiszka, Matt Pinheiro, and Jennifer Mason Funding National Science Foundation Graduation Fellowship, National Defense Science and Engineering Graduation Fellowship, International Society for Reef Studies and the Ocean Conservancy, Earl & Ethel Myers Oceanographic Trust, Jane Miller Scholars, Friends of Hopkins, Woods Institute for the Environment, Center for Ocean Solutions, National Center for Ecological Analysis and Synthesis, and Stanford Department of Biology and My Family Kristin Hunter-Thomson Rob, Margaret, and Maia Pinsky viii Table of Contents Abstract........................................................................................................................... v Acknowledgements ......................................................................................................vii Table of Contents ..........................................................................................................ix List of Tables...............................................................................................................xiii List of Figures..............................................................................................................xiv Introduction .................................................................................................................... 1 Statement on Multiple Authorship ..................................................................... 5 References .......................................................................................................... 6 Chapter 1: Using isolation by distance and effective density to estimate dispersal scales in anemonefish ..................................................................................... 11 1.1. Abstract...................................................................................................... 11 1.2. Introduction ............................................................................................... 12 1.3. Materials and Methods .............................................................................. 14 1.3.1. Study system..............................................................................
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