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UNIVERSITY of CALIFORNIA, SAN DIEGO Foraging Ecology of North UNIVERSITY OF CALIFORNIA, SAN DIEGO Foraging ecology of North Pacific albacore in the California Current System. A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Oceanography by Sarah M. Glaser Committee in charge: David M. Checkley, Jr., Chair Josh Kohn Mark D. Ohman George Sugihara George Watters Brad Werner 2009 Copyright Sarah M. Glaser, 2009 All rights reserved. The Dissertation of Sarah M. Glaser is approved, and it is acceptable in quality and form for publication on microfilm and electronically: ____________________________________________ ____________________________________________ ____________________________________________ ____________________________________________ ____________________________________________ ____________________________________________ ____________________________________________ Chair University of California, San Diego 2009 iii DEDICATION For his passion to understand the ocean and the creatures who swim within, this dissertation is dedicated to John Lagrange and the memory of his wife, Linda. Without Mr. Lagrange, I might never have decided to study albacore, a powerful and beautiful fish that has taught me an incredible amount. Thank you, John, for your insight and your guidance, for the support of the American Fisherman’s Research Foundation and the commercial albacore industry, and for prioritizing the role of scientific inquiry in management while reminding us of our limitations. This study would not have been possible without you. iv TABLE OF CONTENTS Signature Page……………………………………………………………………………iii Dedication………………………………………………………………………….……..iv Table of Contents…………………………………………………………………………v List of Figures...………………………………………………………………………….vii List of Tables……………………………………………………………………………..xi Acknowledgements………………………………………………………………………xii Vita…….…………………………………………………………………………...……xvi Abstract…………………………………………………………………………………xvii Chapter 1. Introduction……………………………………………………………………1 Theoretical foundation…………………………………………………………….2 Biology of North Pacific albacore………………………………………………...4 Outline of the dissertation…………………………………………………………6 References…………………………………………………………………………9 Chapter 2. Quantifying interdecadal variability in diet habits, prey energetics, and consumption rates of North Pacific albacore in the California Current System…………14 Abstract…………………………………………………………………………..14 Introduction………………………………………………………………………15 Methods…………………………………………………………………………..18 Results……………………………………………………………………………27 Discussion………………………………………………………………………..30 Conclusions………………………………………………………………………40 Tables…………………………………………………………………………….42 Figures……………………………………………………………………………45 Appendix 2.1. Variability in prey energy density values……………...…………54 Appendix 2.2. Sampling in relation to sardine habitat…..………...……………..57 References………………………………………………………………………..58 v Chapter 3. The foraging ecology of North Pacific albacore in the California Current System.…………………………………………………………………………………...67 Abstract…………………………………………………………………………..67 Introduction………………………………………………………………………68 Methods…………………………………………………………………………..72 Results…………………………………………………………………………....83 Discussion………………………………………………………………………..91 Conclusion……………………………………………………………………...108 Tables…………………………………………………………………………...110 Figures…………………………………………………………………………..118 Appendix 3.1. Distribution of albacore predation on prey……………………..131 Appendix 3.2. Genetic sequencing of visually-unidentifiable prey…………….151 References………………………………………………………………………158 Chapter 4. Do albacore exert top-down pressure on Northern anchovy? Estimating mortality of juvenile anchovy as a result of predation by North Pacific albacore.……..165 Abstract…………………………………………………………………………165 Introduction……………………………………………………………………..166 Methods…………………………………………………………………………171 Results…………………………………………………………………………..178 Discussion………………………………………………………………………181 Conclusion……………………………………………………………………...187 Tables…………………………………………………………………………...189 Figures…………………………………………………………………………..191 References………………………………………………………………………204 Chapter 5. Conclusion…………………………………………………………………..209 vi LIST OF FIGURES Chapter 2 Figure 2.1. Distribution of sampling effort for five albacore diet habits studies………...45 Figure 2.2. Length-frequency distribution of albacore from 4 of 5 diet studies, and from commercial logbooks of Eastern Pacific Ocean troll fisheries…………………………..47 Figure 2.3. Length-frequency distribution of fish prey (n = 942) found in juvenile albacore, 2005-2006 (this study)…………………………………………………………48 Figure 2.4. Influence of prey energy density on daily consumption rates of albacore…..49 Figure 2.5. Energetic contribution of common prey items to juvenile albacore diet in the California Current System……………………………………………………………….50 Figure 2.6. A) Calculated annual consumption to biomass ratio (Q:B) for juvenile albacore in the California Current System. B) Ensemble energy density (EDn), weighted according to proximity from two flanking diet studies…………………………………..51 Figure 2.7. Time series of abundance for age-0 (recruitment) anchovy, sardine, hake, and Pacific mackerel………………………………………………………………………….52 Figure A2.2. Sampling in relation to sardine habitat……………………………………57 Chapter 3 Figure 3.1. Distribution of sample collection in summer-fall 2005 and 2006, aggregated by albacore daily sampling unit………………………………………………………...118 Figure 3.2. Species accumulation curves showing the necessary sample size needed to discover the number of species categories given different levels of aggregation………119 Figure 3.3. Total reconstituted mass as a snapshot in time in an albacore stomach..…..120 Figure 3.4. Total energy content as a snapshot in time in an albacore stomach………..121 Figure 3.5. Total protein content as a snapshot in time in an albacore stomach……….122 Figure 3.6. Regional differences in dietary preferences of albacore in the California Current System………………………………………………………………………….123 vii Figure 3.7. Dietary preferences of albacore grouped as 31 independent daily sampling units……………………………………………………………………………………..124 Figure 3.8. Interannual dietary preferences of albacore for 20 species categories of prey……………………………………………………………………………………..125 Figure 3.9. Daily energetic demand for albacore of a given length calculated with a bioenergetics model developed by Essington (2003)…………………………………..126 Figure 3.10. Number of unique prey species categories (unaggregated, n = 59) found in a stomach…………………………………………………………………………………127 Figure 3.11. Feeding strategy of and prey importance of albacore, after Costello 1990…………………………………………………………………………………….128 Figure 3.12. Classification of albacore foraging strategy according to Tokeshi (1991).…………………………………………………………………………………..129 Figure 3.13. Classification of albacore foraging strategy according to Bridcut and Giller (1995)…………………………………………………………………………………..130 Figure A.3.1.1. Stomachs containing Abraliopsis sp………………………………….131 Figure A.3.1.2. Stomachs containing Loligo opalescens………………………………132 Figure A.3.1.3. Stomachs containing Octopoteuthis sp………………………………..133 Figure A.3.1.4. Stomachs containing Gonatus sp……………………………………...134 Figure A.3.1.5. Stomachs containing Onychoteuthis borealijaponica………………...135 Figure A.3.1.6. Stomachs containing Squid (other)……………………………………136 Figure A.3.1.7. Stomachs containing Japatella heathi………………………………...137 Figure A.3.1.8. Stomachs containing Octopus (other)…………………………………138 Figure A.3.1.9. Stomachs containing Decapods……………………………………….139 Figure A.3.1.10. Stomachs containing Euphausiids…………………………………...140 Figure A.3.1.11. Stomachs containing Amphipods……………………………………141 Figure A.3.1.12. Stomachs containing Phronima sedentaria………………………….142 viii Figure A.3.1.13. Stomachs containing Malacostraca………………………………….143 Figure A.3.1.14. Stomachs containing Engraulis mordax…………………………….144 Figure A.3.1.15. Stomachs containing Merluccius productus…………………………145 Figure A.3.1.16. Stomachs containing Cololabis saira………………………………..146 Figure A.3.1.17. Stomachs containing Myctophids……………………………………147 Figure A.3.1.18. Stomachs containing Sebastes spp…………………………………..148 Figure A.3.1.19. Stomachs containing Sardinops sagax………………………………149 Figure A.3.1.20. Stomachs containing Fishes (other)………………………………….150 Chapter 4 Figure 4.1. Age composition of landings in major fisheries for albacore in the North Pacific Ocean…………………………………………………………………………...191 Figure 4.2. Indices of relative abundance of albacore caught by two major fisheries…192 Figure 4.3. 1 degree x 1 degree cells used to estimate albacore abundance in the California Current System……………………………………………………………..193 Figure 4.4. Estimates of albacore biomass in the California Current System………….194 Figure 4.5. Index of relative abundance of albacore in the California Current System in three regions…………………………………………………………………………….195 Figure 4.6. Estimates of albacore biomass in three regions of the CCS………………..196 Figure 4.7. Seasonal distribution of albacore in the CCS from standardized CPUE data……………………………………………………………………………………..197 Figure 4.8. Annual albacore consumption of anchovy in the California Current System and human landings……………………………………………………………………198 Figure 4.9. Size of anchovy found in albacore stomachs by month, collected in 2005 and 2006……………………………………………………………………………………199 ix Figure 4.10. Calculated biomass of anchovy recruitment (young of year fish) for the central Northern anchovy stock in the CCS……………………………………………200 Figure 4.11. Proportion of young of year Northern anchovy in the central stock consumed by albacore……………………………………………………………………………...201 Figure 4.12. Instantaneous mortality rate on
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