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DISSERTATION March2006 © Copyright by Alexander Whitman Miller 2000 UNIVERSITY OF CALIFORNIA Los Angeles Assessing the Importance of Biological Attributes for Invasion Success: Eastern Oyster (Crassostrea virginica) Introductions and Associated Molluscan Invasions of Pacific and Atlantic Coastal Systems A dissertation submitted in partial satisfaction of the requirements for the degree Doctor of Environmental Science and Engineering by Alexander Whitman Miller 2000 SIGNATURE PAGE The dissertation of Alexander Whitman Miller is approved. ______________________________ Richard R. Vance ______________________________ Michael D. Collins ______________________________ L. Donald Duke _______________________________ Richard F. Ambrose, Committee Chair University of California, Los Angeles 2000 ii DEDICATION This dissertation is dedicated to my mother, Jessie Barr Miller, who instilled me with an interest in nature and a sense of stewardship, and to my wife, Melissa Hagan, who has always encouraged me to pursue my goals and generously provided support for me to do so. iii TABLE OF CONTENTS SIGNATURE PAGE ................................................................................................II DEDICATION......................................................................................................... III TABLE OF CONTENTS .......................................................................................IV LIST OF FIGURES ................................................................................................IX LIST OF TABLES..................................................................................................XI ACKNOWLEDGEMENTS ..................................................................................XII VITA ......................................................................................................................XIII PUBLICATIONS AND PRESENTATIONS...................................................XIV ABSTRACT OF THE DISSERTATION ....................................................... XVII CHAPTER 1 ..............................................................................................................1 INTRODUCTION.....................................................................................................1 LITERATURE CITED.............................................................................................8 CHAPTER 2 ............................................................................................................12 iv HISTORICAL REVIEW OF THE EASTERN OYSTER (CRASSOSTREA VIRGINICA) FISHERY IN THE UNITED STATES AS A VECTOR FOR ACCIDENTAL TRANSPORT OF ASSOCIATED MOLLUSKS...............................................................................................................12 INTRODUCTION...................................................................................................13 TERMINOLOGY....................................................................................................14 NATURAL HISTORY OF CRASSOSTREA VIRGINICA.............................15 HISTORY OF THE EASTERN OYSTER FISHERY.......................................16 Important Oystering Locations in the Mid-Atlantic and New England...................... 17 The Chesapeake Bay Commercial Oyster Industry.................................................. 18 The Commercial Oyster Industry of New York City................................................. 21 Oyster Seed, the Link between Chesapeake Bay and Embayments to the North ......... 23 Foreign Export and Intercontinental Transport of Eastern Oysters.......................... 26 Oyster Fishery Practices....................................................................................... 30 SUMMARY.............................................................................................................34 LITERATURE CITED...........................................................................................40 CHAPTER 3 ............................................................................................................48 DISCRIMINATING AMONG SUCCESSFUL AND FAILED MOLLUSCAN INVADERS: A RETROSPECTIVE ANALYSIS OF OYSTER-MEDIATED INTRODUCTIONS TO SAN FRANCISCO BAY.........................................................................................................................48 v ABSTRACT.............................................................................................................48 INTRODUCTION...................................................................................................50 Crassostrea virginica - A vector for invertebrate introductions................................ 52 METHODS ..............................................................................................................56 Molluscan Oyster Associates................................................................................. 56 Biogeographical, Life History, and Habitat Characteristics of Oyster Associates ..... 59 Categorical Variables........................................................................................... 61 Continuous Numerical Variables........................................................................... 64 Statistical Tests.................................................................................................... 68 Univariate Tests ................................................................................................... 69 Multivariate Tests................................................................................................. 71 RESULTS.................................................................................................................72 Univariate Analyses.............................................................................................. 72 Discriminant Analyses .......................................................................................... 76 DISCUSSION..........................................................................................................80 Differentiating Successful and Failed Invaders....................................................... 80 Two Notable Invasion Failures.............................................................................. 88 Predicting Invasion Success – The Tens Rule ......................................................... 93 CONCLUSION .......................................................................................................95 vi APPENDIX 3.1. BIOLOGICAL ATTRIBUTES OF MOLLUSKS. ERROR! BOOKMARK NOT DEFINED. LITERATURE CITED.........................................................................................121 CHAPTER 4 ..........................................................................................................136 COMPARING OYSTER-MEDIATED MOLLUSCAN INTRODUCTIONS TO THE COASTS........ 136 OF THE EASTERN PACIFIC AND EASTERN ATLANTIC OCEANS..................................... 136 INTRODUCTION.................................................................................................136 Molluscan Invaders of the Northeast Atlantic ........................................................138 Repeated Invasions of Multiple Coasts – Are Marine Invasions Random? ...............139 Oyster-mediated Molluscan Invaders of Northwest Europe with Comparisons to North west Pacific Invasions .................................................................................143 Patterns of Oyster-Mediated Molluscan Invasions of the Northeast Atlantic and Northeast Pacific .................................................................................................157 Differences in Oyster Introductions to Europe and the West Coast .........................159 DISCUSSION........................................................................................................160 APPENDIX 4.1. MATHEMATICAL COMBINATIONS.............................169 LITERATURE CITED.........................................................................................171 CHAPTER 5 ..........................................................................................................179 BIOLOGICAL INVASIONS: THE CHALLENGES AHEAD ................................................. 179 vii A MODEST BEGINNING..................................................................................181 AREAS FOR FUTURE RESEARCH................................................................183 In Situ Investigations of Invaders and Recipient Environments...............................184 Invasions Research and Management...................................................................185 LITERATURE CITED.........................................................................................190 viii LIST OF FIGURES Chapter 2 2.1 Global oyster transport..................................................................................36 2.2 Commercially important oystering centers of mid-Atlantic and northeastern United States. ................................................................................................37 Chapter 3 3.1 Global oyster transport..................................................................................97 3.2a Native range, Boonea bisuturalis..................................................................98 3.2b Native range, Busycotypus canaliculatus......................................................98 3.2c Native range, Crepidula convexa..................................................................99 3.2d Native range,
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